microcosm experiment drought

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Drought shifts soil nematode trophic groups and mediates the heterotrophic respiration

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Cancan Zhao, Yuanhu Shao, Huijie Lu, Aimée T Classen, Zuyan Wang, Ying Li, Yanchun Liu, Zhongling Yang, Guoyong Li, Shenglei Fu, Drought shifts soil nematode trophic groups and mediates the heterotrophic respiration, Journal of Plant Ecology , Volume 17, Issue 2, April 2024, rtae012, https://doi.org/10.1093/jpe/rtae012

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As the most diverse metazoan taxa, soil nematodes serve a diversity of functions in soil food webs and thus can regulate microbial community composition and affect organic matter decomposition and nutrient turnover rates. Because nematodes depend on water films to access food resources, drought can negatively affect nematode–microbial food webs, yet the impacts of drought on nematode diversity and abundance and how these changes may influence food web members and their functions are hardly explored. Here, we coupled research along a drought gradient in arid and semiarid grasslands with a detailed intact plant–soil microcosm experiment to explore the patterns and mechanisms of how drought impacts nematode abundance and carbon footprint, microbial phospholipid fatty acid (PLFA) and heterotrophic soil respiration. Overall, in the field and the microcosm experiments, we found that nematode abundance, carbon footprint and diversity, microbial PLFA and heterotrophic respiration were reduced under drier conditions. In addition, drought altered nematode and microbial community composition, through reducing the nematode channel ratio and increasing the relative fungivorous nematode abundance and the fungal to bacterial ratio. The soil decomposition channel shifted from a bacterial to a fungal pathway in response to drought, indicating decelerated heterotrophic respiration under drought. These results highlight the important contribution of soil nematodes and their associated microbial food web to soil carbon cycling. Our findings underscore the need to incorporate key soil fauna into terrestrial ecosystem model evaluation.

土壤线虫作为最多样的后生动物类群，在土壤食物网中发挥着多种功能，可以调节微生物群落组成，影响有机质分解和养分周转速率。由于线虫依赖水膜获取食物资源，干旱会对线虫-微生物食物网产生负面影响，但干旱对线虫多样性和丰度的影响以及这些变化如何影响食物网成分及其功能的研究还较少。在本研究中，我们将干旱和半干旱草原的干旱梯度研究与原位植物-土壤微宇宙实验相结合，探讨干旱影响线虫丰度和碳足迹、微生物磷脂脂肪酸以及土壤异养呼吸的模式和机制。在野外调查和微宇宙实验中，我们发现线虫丰度、碳足迹、多样性、微生物磷脂脂肪酸和异养呼吸在干燥条件下均有下降。干旱通过降低线虫通道比、增加食真菌线虫相对丰度和真菌/细菌比，改变了线虫和微生物群落组成。在干旱条件下，土壤分解途径由细菌通道向真菌通道转化，表明干旱条件下异养呼吸速率减慢。我们的研究结果强调了土壤线虫及其相关微生物食物网对土壤碳循环的重要贡献，也强调了将关键土壤动物纳入陆地生态系统模型评估的必要性。

Climate models predict that the occurrence, intensity and extent of drought are increasing around the globe ( IPCC 2021 ). Drought significantly affects plant growth, soil biodiversity and ecosystem carbon (C) cycling by reducing soil moisture availability ( de Vries et al. 2012 ; Eisenhauer et al. 2012 ; Franco et al. 2019 ). The effects of drought can be particularly pronounced in arid and semiarid grasslands ( Nielsen and Ball 2015 ; Zhang et al. 2022 ; Zhao et al. 2016 ).

Soil respiration is an important C feedback in the global C cycle, releasing 10 times more CO 2 than fossil fuel combustion ( Bond-Lamberty and Thomson 2010 ; Diao et al. 2022 ). Around half of soil respiration is heterotrophic respiration, which is the release of CO 2 from the soil to the atmosphere through the decomposition of organic matter by soil microbes and fauna ( Bond-Lamberty 2018 ; Nielsen et al. 2011 ). Because soil microorganisms are directly responsible for the vast majority of organic matter decomposition, soil C cycle models have emphasized the crucial role of microorganisms and enzyme activity ( Deng et al. 2021 ; Fan et al. 2021 ; Sulman et al. 2018 ). However, the respiration of soil fauna, especially nematodes, should also be included in these models, because soil faunal respiration is comparable to 15% of the global C emissions from fossil fuel utilization ( van den Hoogen et al. 2019 ). Given the importance of soil fauna in C emissions, more attention needs to be paid to their response to climatic and environmental drivers in experiments and models.

Soil nematodes account for an estimated four-fifths abundance of multicellular animals on earth ( van den Hoogen et al. 2019 ). Thus, soil nematodes are good indicators of biological activity under drought stress because they rely on water films around soil particles ( Wang et al. 2021 ; Xiao et al. 2021 ). The metabolic footprint, i.e. C footprint, encompasses nematode production and respiration and provides an effective method for estimating the contribution of nematodes to C emissions ( Ferris 2010 ). In addition, soil nematodes occupy multiple trophic categories, including bacterivores, fungivores, herbivores, omnivores and predators. Nematodes, bacteria and fungi can interact to regulate organic matter decomposition and C cycling ( Jiang et al. 2018 ; Luo et al. 2021 ). Bacterial communities are often sensitive to drought because of their higher dependence on water. Fungi, in contrast, can reach pockets of water through air-filled soil pores, and therefore they are more resistant to drought ( Vandegehuchte et al. 2015 ). Fungivorous nematodes may be less impacted by drought because their fungal prey should be relatively stable under drought conditions ( Landesman et al. 2011 ). The energy channel theory posits that the fungal-based energy channel is slow and conservative, whereas the bacterial-based system is fast and recycles nutrients quickly, facilitating leaching and nutrient loss from the ecosystem ( Rooney et al. 2006 ). Therefore, drought may alter the nematode–microbial energy channel and then slow down C release.

More than a third of Earth’s land surface area is classified as arid to semiarid grasslands, where the main constraint on biological activity is water availability ( Collins et al. 2008 ; Nielsen and Ball 2015 ). Here, we coupled a field survey along a drought gradient in arid and semiarid grasslands in northern China with an intact plant–soil microcosm experiment that manipulated precipitation in a regression design. The objectives of the study were 2-fold. We explored how drought influenced the soil food web community and their activity with a focus on soil nematodes using a gradient of arid and semiarid grassland sites. Next, we experimentally manipulated drought conditions on intact plant–soil microcosms to better understand how drought and the changing soil food web altered C release. We propose the first hypothesis that drought would decrease soil nematode abundance and diversity due to water film and nutrient depletion. Given that soil fungi, and thus fungivorous nematodes are likely drought tolerant, we test the second hypothesis that drought would increase the relative dominance of fungal pathways in the soil food web and decrease the relative dominance of bacterial pathways. Moreover, we hypothesized that except soil microbes, soil nematodes would be important in mediating heterotrophic respiration.

Field survey experiment and soil sampling

We surveyed three arid and semiarid grassland sites in Inner Mongolia of China, including Duolun County (low drought site), Zhengxiangbai Banner (medium drought site) and Sunitezuo Banner (high drought site, see Li et al. 2017 for map). Long-term mean annual precipitation at the three sites is 385, 326 and 223 mm, respectively, forming a natural drought gradient ( Table 1 ). The vegetation types of all the three sites are similar, which are dominated by Stipa krylovii and Artemisia frigida . The soil at the three sites is classified as Haplic Calcisols according to the Food and Agricultural Organization classification ( Li et al. 2017 ).

Description of the three study field sites

Abbreviations: ET = evapotranspiration, MAP = mean annual precipitation, MAT = mean annual temperature, N = nitrogen, P = phosphorus.

We established four sampling plots (20 m × 20 m) at each of the three sites (4 within site plots × 3 sites = 12 total plots). All plots were free from human disturbance. The distance between any two plots was more than 1 km. In early August 2015, we sampled soil using 5 cm diameter corers to a 10-cm depth from all of the 12 plots. Within each plot, five cores were randomly collected and combined into a composite sample. After visible plant roots removed, the soil was passed through a 2-mm sieve. All samples were then stored at 4°C until we extracted and fixed nematodes the next day.

Microcosm experiment and soil sampling

In August of 2015, we established a microcosm experiment by extracting 24 intact soil and plant columns (using PVC tube of 15 cm diameter and 10 cm depth, uniform plant coverage) from the Duolun County site, the low drought location along our transect, and transported them back to greenhouse to keep the intact microcosm plants alive. These columns have similar soil biological community and properties. Next, using a single factor design, four precipitation manipulations were established, ambient control which was equal to 100% of the annual of precipitation added (100%P, 385 mm), 80% of the annual precipitation addition (80%P, 308 mm), 60% of the annual precipitation addition (60%P, 231 mm) and 40% of the annual precipitation addition (40%P, 154 mm). Distilled water was added by spraying every week on average as prescribed in the above treatments ( n  = 6). All intact soil and plant columns were placed in a greenhouse (~10°C) with transparent roofs to keep natural light for 1 year. We harvested the experiment in August of 2016. We removed all roots and sieved the soil 2-mm prior to nematodes and phospholipid fatty acids (PLFAs) extraction, soil respiration measurements and soil property analysis.

Nematode community analysis

We treated soils collected in the observational and microcosm experiments in the same way. Nematodes were extracted from 100 g of fresh soil immediately using a modified Baermann funnel method ( Ruess 1995 ), and then fixed in 4% formalin until further identification. Total nematode abundance was counted in each sample. The first 100 nematodes encountered were identified to genus using a DIC microscope (Eclipse 80i, Nikon, ×100). The nematodes were classified into four trophic groups: bacterivores, fungivores, herbivores and omnivore–predators.

Nematode biomass C was calculated by multiplying the abundance of each genus by their fresh weight, using a fresh to dry weight ratio of 0.20 and a C content of 52% dry weight ( Ferris 2010 ). The mean fresh weight of nematode genera was employed from the ‘Nemaplex’ database ( http://nemaplex.ucdavis.edu/ecology/ecologymenu.htm ) developed by Howard Ferris. Nematode C footprint ( F ) was calculated to assess the amount of C and energy entering the soil food web using the sum of nematode production and respiration as follows:

where N t is the number of individuals in each of the t genus, W t and m t are the body weight and the c-p of t genus, respectively ( Ferris 2010 ). Nematode channel ratio (NCR), which represents the relative contributions of bacterivore and fungivore nematodes, was calculated as follows:

where Ba and Fu are bacterivore and fungivore nematode abundance, respectively ( Bongers and Bongers 1998 ). To assess the diversity of nematode community, Shannon’s diversity index ( Hʹ ) was calculated as follows:

where pi is the proportion of the i th genus.

PLFA analysis

PLFA analysis was used to quantify the markers for microbial biomass and calculate the fungal to bacterial ratio ( Frostegård et al. 2011 ). Lipids were extracted using a chloroform–methanol–phosphate buffer mixture (1:2:0.8), and then using a silicic acid column separated them into neutral lipids, glycolipids and phospholipids ( Zelles 1999 ; Zhao et al. 2015 ). PLFA was analyzed using a gas chromatograph (Agilent 7890A, Agilent Technologies, USA) and a Microbial Identification System (MIDI Inc., USA).

Total PLFA was used as a measurement of microbial biomass. Bacterial biomass was estimated by the summed concentration of the mono-unsaturated, cyclopropyl and branched PLFAs, including 16:1ω7, 17:1ω8, 18:1ω7, cy17:0, cy19:0, i15:0, a15:0, i16:0, i17:0 and a17:0. Fungal biomass was determined by 18:2ω6 and 18:1ω9.

Soil and plant properties and heterotrophic respiration

Gravimetric soil moisture was measured by oven-drying soils for 24 h at 105°C. Soil organic C was measured using the solid combustion method with an elemental analyzer (Elementar vario MACRO CUBE, Elementar Co., Hanau, Germany). Plant coverage was visually estimated when harvest. For heterotrophic respiration measurement, fresh soil of 20 g was placed in a 500-ml glass flask with a connecting tube. A 5-ml of 0.05 M NaOH solution was then injected into the connecting tube to absorb the CO 2 released from the soil in the flask. The glass flasks were incubated at 25°C in the dark for 14 days. Heterotrophic respiration was then determined using an alkali absorption of CO 2 followed by titration of the residual OH − with a standardized HCl solution ( Zhao et al. 2016 ).

Statistical analysis

Prior to statistical analysis, the data were tested for normality and homogeneity of variance. Data were analyzed with a one-way ANOVA to determine the effects of drought on all variables. The multiple comparisons (LSD) based on the ANOVA were used to compare the differences of all variables among treatments. Statistical analyses were performed using IBM SPSS 26.0 (SPSS Inc., Chicago, IL, USA). Structural equation model (SEM) was used to test the causal relations among soil moisture, C pools, energy channel and C fluxes. The variables were log transformed before conducting the SEM analysis to mitigate departures from normality and linearity if necessary. The SEM analysis was performed with SPSS AMOS 26.0 (IBM Corp., Armonk, NY, USA) software using maximum likelihood estimation procedures.

Soil nematode in the field survey experiment

In the observational field survey, a total of 78 nematode genera were collected ( Supplementary Table S1 ). The medium drought and the high drought site had 58% and 31% lower of soil nematode abundance, 71% and 67% lower of nematode biomass and 70% and 58% lower of C footprint than the low drought site ( Fig. 1a–c ). There was a negative relationship between aridity and NCR as well as between aridity and the diversity index ( Fig. 1d and e ). Nematode genus richness at the medium and high drought site had a decreasing trend than the low drought site but not significant ( Fig. 1f ). Relative bacterivore and fungivore abundance increased 2.0- and 2.5-folds in the high drought site than the low drought site ( Fig. 1g ).

Soil nematode abundance (a), biomass (b), carbon footprint (c), NCR (d), diversity index (e), genus richness (f) and trophic group percentage (g) at three sites in the field survey experiment. Different lowercase letters indicate significant differences among sites. Abbreviations: H = high drought site, L = low drought site, M = medium drought site.

Soil nematode in the microcosm experiment

The abundance, biomass and C footprint of nematodes in the microcosm experiment decreased with drought ( Fig. 2a–c ). The 80%P, 60%P and 40%P treatment reduced soil nematode abundance by 48%, 73% and 77%, nematode biomass by 66%, 87% and 86% and C footprint by 61%, 85% and 87%, respectively. NCR and diversity index decreased along the drought gradient but not significantly ( Fig. 2d and e ). All drought treatments significantly reduced nematode genus richness ( Fig. 2f ). 40%P treatment increased relative fungivore abundance ( Fig. 2g ).

Soil nematode abundance (a), biomass (b), carbon footprint (c), NCR (d), diversity index (e), genus richness (f) and trophic group percentage (g) along a drought gradient in the microcosm experiment. Different lowercase letters indicate significant differences among treatments.

Microbial PLFA, soil and plant properties and heterotrophic respiration in the microcosm experiment

All drought treatments reduced microbial total PLFA ( Fig. 3a ). 80%P, 60%P and 40%P treatment decreased microbial PLFA by 33%, 51% and 30%, respectively. The fungal to bacterial PLFA ratio increased slightly along the drought gradient but not significantly ( Fig. 3b ).

Soil microbial total PLFA (a) and the fungal to bacterial PLFA ratio (b) along a drought gradient in the microcosm experiment. Different lowercase letters indicate significant differences among treatments.

Soil moisture, heterotrophic respiration and plant coverage declined with the drought gradient, and reached the minimum under the 40%P treatment ( Fig. 4a , c and d ). 80%P, 60%P and 40%P treatment suppressed soil moisture by 8%, 29% and 58%, inhibited heterotrophic respiration by 21%, 58% and 71% and decreased plant coverage by 27%, 42% and 75%, respectively. There was no obvious change in soil organic C ( Fig. 4b ).

Soil moisture (a), soil organic carbon (b), heterotrophic respiration (c) and plant coverage (d) along a drought gradient in the microcosm experiment. Different lowercase letters indicate significant differences among treatments.

Relations among soil moisture, C pools, energy channel and C fluxes

The SEM provided a good fit to the data ( χ 2  = 12.5, df = 17, P  = 0.767, CFI = 0.999, GFI = 0.883, RMSEA = 0.000). Soil moisture was the only exogenous variable in the model. Decreased soil moisture reduced nematode biomass, C footprint, NCR and enhanced the fungal to bacterial PLFA ratio, thereby suppressed heterotrophic respiration directly and indirectly ( Fig. 5 ). The model explained 78% and 21% of the variances in heterotrophic respiration and soil organic C, respectively.

SEM linking soil moisture, carbon pools, energy channel and carbon fluxes ( χ 2  = 12.5, df = 17, P  = 0.767, CFI = 0.999, GFI = 0.883, RMSEA = 0.000). Solid arrows indicate causal relationships among measured variables. Dashed arrow indicates a non-significant relationship. Numbers next to the arrows are standardized regression coefficients. The model R 2 for each endogenous variable is presented next to the variable. Abbreviations: BN = biomass of nematode, CFN = carbon footprint of nematode, F/B = fungal to bacterial PLFA ratio, HR = heterotrophic respiration, SM = soil moisture, SOC = soil organic carbon.

Effects of drought on soil nematode community

We combined an observational study along an extensive precipitation gradient with a precipitation manipulation using intact plant–soil microcosms to explore how drought impacts soil food webs and their functions. Supporting previous work, our result indicates that nematodes respond strongly with drought as water becomes limited ( Wang et al. 2021 ; Xiong et al. 2020 ; Yan et al. 2018 ; Zhao et al. 2018 ). Across both studies, drought reduced nematode abundance up to 77%, biomass up to 87% and their C footprint up to 87% ( Figs 1 and 2 ) relative to control, or site that had the highest soil moisture. We hypothesized that nematodes may respond negatively to drought for reductions in soil water films which change their movement and thus access to the food that sustains their growth ( Landesman et al. 2011 ; Olatunji et al. 2019 ). Alternatively, reduced water availability can also suppress plant production, nutrient availability and microbial biomass at the base of the food web ( Figs 3 and 4 ) leading to nutrient-depleted conditions that inhibit nematodes growth ( Franco et al. 2019 ; Guo et al. 2021 ; Zhou et al. 2022 ). Our first hypothesis of water film and nutrient depletion has been verified in this study.

In line with our second hypothesis, drought decreased NCR and enhanced the relative fungivore abundance. Thus, drought can increase the relative dominance of fungal pathways and decrease the dominance of bacterial pathways, which cause a switch from the bacterial-based to the fungal-based energy channel. Soil fungi are often more resistant to drought conditions than bacteria, because fungal hyphal network can transfer moisture from water-filled micropores to dry pores spaces; whereas, bacteria cannot move moisture around the soil matrix and require water films for motility and substrate diffusion ( Zhang et al. 2020 ; Zhao et al. 2016 ). Fungivorous nematodes may, therefore, be less impacted by drought because the fungi they feed on are more drought tolerant ( Vandegehuchte et al. 2015 ). In this study, fungivore nematode abundance of Aphelenchoides , Aphelenchus and Tylencholaimus genera were stable across the different moisture conditions, which have proved the above view. Surprisingly, we found no significant effect of drought on relative omnivore–predator nematode abundance. These large-bodied nematodes require thick water films for movement and thus are often responsive to drought conditions ( Sylvain et al. 2014 ; Vandegehuchte et al. 2015 ). Perhaps in xeric ecosystems, like the ones studied here, omnivorous and predatory nematodes have adapted dehydration survival strategies ( Ankrom et al. 2022 ; Franco et al. 2019 ). We also found that drought shifted nematode community composition by decreasing both diversity index and genus richness, i.e. the loss of rare taxa ( Franco et al. 2022 ).

Regulation of soil nematode community on C cycling

The results of SEM showed a significant causal relationship between nematode C footprint and heterotrophic respiration. The relationship indicates that nematodes play an important role in modulating soil C cycling, which is in accord with the third hypothesis. Soil fauna contribute between 1% and 25% of total heterotrophic respiration ( Jiang et al. 2016 ; Persson 1989 ), while soil nematodes make up a large fraction of the soil fauna pool. Thus, changes in nematode C footprint may have a larger impact on terrestrial CO 2 release than expected ( Nielsen et al. 2011 ). Prior work in soil microcosms also found that the addition of nematodes to soil increased CO 2 emission by 17%, therefore, reductions in nematode abundance or C footprint can decrease soil C fluxes ( Zaitsev et al. 2018 ).

Nematodes can impact microbial food web structure as well as heterotrophic respiration via their prey on soil microorganisms. Via predation, nematodes could reduce microbial biomass as well as respiration ( Cardoso et al. 2016 ; Zhou et al. 2019 ); however, by increasing microbial turnover and thus nitrogen cycling, heterotrophic respiration may be stimulated ( Chen and Ferris 1999 ; Ferris et al. 1998 ; Fu et al. 2005 ; He et al. 2022 ). The trade-off between these two processes can lead to a stimulation or reduction of soil respiration. We found that drought decreased nematodes, microbial biomass and heterotrophic respiration suggesting that the first hypothesis—suppressed substrate availability—is at play. Microbial food web structure showing a more fungal-dominated energy channel under drought stress, suggests that drought would slow down the energy flow of the soil microbial food web ( Xue et al. 2021 ; Zhao et al. 2019 , 2021 ). Previous study also has proved that the per unit biomass of fungi respired out less CO 2 than bacteria ( Six et al. 2006 ).

In summary, soil nematodes provide a sensitive tool for evaluating the effect of drought on ecosystem function and potential C feedback. Drought reduced soil nematode abundance, biomass and C footprint, altered nematode and microbial community composition, and directly and indirectly suppressed heterotrophic respiration. Our results suggest that extreme drought, which is predicted to increase in this already xeric grassland region, would decelerate C decomposition. Our results underscore the need to incorporate key soil fauna into terrestrial ecosystem model evaluation—especially in areas that are suspectable to extreme climate events, such as xeric grassland.

Supplementary material is available at Journal of Plant Ecology online.

Table S1: List of the identified nematode genera in the three study field sites.

This work was supported by the National Natural Science Foundation of China (32371737, 32130066, 31971454, 31971534), Natural Science Foundation of Henan Province (232300420004) and Xinyang Academy of Ecological Research Open Foundation (2023DBS10).

Conflict of interest statement . The authors declare that they have no conflict of interest.

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Drought shifts soil nematodes to smaller size across biological scales

• Laboratory of Nematology

Research output : Contribution to journal › Article › Academic › peer-review

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• 10.1016/j.soilbio.2023.109099
• https://edepot.wur.nl/633126 Licence: Taverne

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• Soil Nematodes Agricultural and Biological Sciences 100%
• Body Size Agricultural and Biological Sciences 100%
• Nematode Immunology and Microbiology 100%
• Progeny Agricultural and Biological Sciences 25%
• Offspring Agricultural and Biological Sciences 25%

T1 - Drought shifts soil nematodes to smaller size across biological scales

AU - Lu, Leilei

AU - Li, Gen

AU - He, Nianpeng

AU - Li, Huixin

AU - Liu, Ting

AU - Li, Xianping

AU - Whalen, Joann K.

AU - Geisen, S.A.

AU - Liu, Manqiang

PY - 2023/9

Y1 - 2023/9

N2 - Drought events are increasingly affecting the planet's biodiversity. While shrinking body size in response to drought has been observed in many vertebrate animals, whether this rule applies to microscopic animals and the mechanisms during this process remains largely unknown. To address this knowledge gap, we conducted a regional-scale investigation and a microcosm experiment to systematically evaluate the impact of drought stress on the body size of the most abundant soil animals on Earth – nematodes – across various biological scales, including community, population and individual levels. Our results showed that nematode body size declined with drought stress at all biological scales, including a community shift toward smaller-sized species, a smaller body size at the population scale, and a decrease in size-at-age of individuals. Additionally, we designed a petri dish experiment to examine the reversible plasticity of body size under drought stress using a drought-tolerant nematode species. We found that while nematode body size could not be fully reversed when drought stress was alleviated in the offspring generation, offspring from parents that experienced severe drought conditions could acquire tolerance, leading to a relatively smaller reduction in overall body size compared to those from parents that suffered no or light drought conditions. Overall, our study suggests that the increasing frequency of drought events at the global scale will lead to a reduction in soil nematode body size, potentially causing far-reaching consequences for additional changes in the climate, as well as nutrient cycling in soils.

AB - Drought events are increasingly affecting the planet's biodiversity. While shrinking body size in response to drought has been observed in many vertebrate animals, whether this rule applies to microscopic animals and the mechanisms during this process remains largely unknown. To address this knowledge gap, we conducted a regional-scale investigation and a microcosm experiment to systematically evaluate the impact of drought stress on the body size of the most abundant soil animals on Earth – nematodes – across various biological scales, including community, population and individual levels. Our results showed that nematode body size declined with drought stress at all biological scales, including a community shift toward smaller-sized species, a smaller body size at the population scale, and a decrease in size-at-age of individuals. Additionally, we designed a petri dish experiment to examine the reversible plasticity of body size under drought stress using a drought-tolerant nematode species. We found that while nematode body size could not be fully reversed when drought stress was alleviated in the offspring generation, offspring from parents that experienced severe drought conditions could acquire tolerance, leading to a relatively smaller reduction in overall body size compared to those from parents that suffered no or light drought conditions. Overall, our study suggests that the increasing frequency of drought events at the global scale will lead to a reduction in soil nematode body size, potentially causing far-reaching consequences for additional changes in the climate, as well as nutrient cycling in soils.

U2 - 10.1016/j.soilbio.2023.109099

DO - 10.1016/j.soilbio.2023.109099

M3 - Article

SN - 0038-0717

JO - Soil Biology and Biochemistry

JF - Soil Biology and Biochemistry

M1 - 109099

Biological Role of Trace Elements and Viral Pathologies

• Published: 16 February 2022
• Volume 60 , pages 137–153, ( 2022 )

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• V. V. Ermakov 1 &
• L. N. Jovanović 2  

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The review presents summarized information on a new research avenue in biogeochemistry and geochemical ecology: relationships between the microcosm (viruses) and manifestations of animal and human pathologies. Some aspects of the biological action of selenium, zinc, copper and iodine, their influence on the manifestation and course of viral infections are considered. Attention is focused on the antioxidant, membrane-protective, boosting immunity, hormonal functions of trace elements, and on the antibacterial and antiviral properties of metallic copper and its compounds. The criteria currently applied in assessing the Se status of territories are compared with the incidence of COVID-19 and HIV in the population of the Russian Federation. In some cases, selenium deficiency in the environment is shown to be associated with a higher susceptibility to RNA viral infections. Emphasis is put on the necessity of improving the criteria for assessing the trace element status of territories and further studies in the geochemical ecology of viruses and their role in the biosphere.

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INTRODUCTION

In the context of the discovery of bacteriophage as a new form of living matter, V.I. Vernadsky wrote: “Studies of bacteriophages uncover new manifestations of life on in the biosphere. First, these studies definitely indicate that some organisms can be even smaller than bacteria and possess even greater geochemical energy” (Vernadsky, 1940), and “life reaches here again it possible limit”. V.I. Vernadsky stressed therein not only the importance of the discovery of ultramicroorganisms but also their ability to be involved in the biogenic migration of matter.

Other parasitic substances of the world of living organisms turned out to be viruses. They were discovered by D.I. Ivanovsky in 1892, when he studied the pathologies of tobacco leaves: the tobacco mosaics. The pathologies were proved to be caused by a substance that could pass through the pores of filters and characterized by infectivity. Further studies have proved that this substance was not of bacterial nature and was smaller than bacteria (Ivanovsky, 1892). This was a newly discovered agent of disease, which was later named virus by Martinus Beijerinck (Beijerinck, 1898).

According to V.M. Zhdanov, viruses (regnum Virae ) are obligate intracellular parasites that are widespread among vertebrate and invertebrate animals and among plants, protozoans, fungi, bacteria, and archaea. Viruses are devoid of metabolic conversion and receive energy owing to the metabolism of the host cell. In spite of their small size (20 to 400 nm), viruses are a life form in the proper sense of the word, they carry genetic material, are able to reproduce themselves, show variability (both genetic and phenotypical), and evolve through natural selection. Their variability is maintained by genom variations and as a result of recombination, genetic reassortment, under impacts of the environment, and in interactions with the host organisms and other viruses (Zhdanov et al., 2012). Some viruses of insects can regulate the sizes of the insect populations and are able to pass into a latent state (Ermakova and Tarasevich, 1968).

The biological microworld thus comprises not only “usual” organisms, such as bacteria, fungi, actinomycetes, and ultramicrobacteria (Archaea, Actinibacteria, Cytophaga, and Proteobacteria) but also the realm of viruses ( Virae ), which is widespread in the biosphere. The contents of ultramicroorganisms in soils are very high an may reach dozens to hundreds of million cells per 1 g of soil (Lysak et al., 2010).

In spite of the rocketing progress in virology, genetics, and molecular biology, the roles of viruses in the lives of organisms, ecology, evolution of the biosphere, and geochemical impacts are understood still inadequately poorly.

Nowadays the humankind more and more suffers from the adverse effects of accelerating technological progress. These effects resulted in numerous ecological problems, such as acid rains, ozone holes, environmental pollution with harmful and hazardous chemical elements and toxic compounds, as well as the deficiency of vitally important trace elements in biogeochemical food chains, which gives rise to pandemic diseases and new viral pathologies, which have not been known previously. The latter include the acquired immune deficiency syndrome (AIDS), various types of viral hepatitis, Ebola and Coxsackie’s diseases, cattle rabies, syndromes and diseases induced by the avian influenza virus (SARS-1) and coronavirus (SARS-2; COVID-19), and Kawasaki’s disease in children (Jovanović and Ermakov, 2020).

Mechanisms through which global biospheric changes are related to some diseases are still largely uncertain, and this makes it much more difficult to undertake adequate countermeasures and synthesize new medications to cure these diseases. At the same time, some progress has been achieved in this field over the past two decades.

This publication focuses on the still poorly explored field of geochemical ecology: interrelations between viral pathologies and microelementoses.

Ecological Reasons for a Selenium Deficiency

It is widely known that air is most strongly polluted by industrial facilities and processes: combustion of hydrocarbons (and hence, ash production) for producing energy accompanied by exhausts from various engines (including cars, trucks, planes, motorbikes, etc.). A decrease in Se concentration in blood serum was found in humans living in large industrially developed population centers and the personnel at facilities of the chemical industry (Golubkina et al., 2017).

The three major reasons for selenium deficiency in soils are as follows. Acid rains caused by high sulfur and nitrogen concentrations in the air change the ability of the soils to bind chemically active elements. A change in the pH balance makes some chemical elements more biologically available (these are mostly toxic elements), whereas others (such as Se, Zn, and Mg) become less biologically available. The acidification of soils and natural waters may increase the incidence of cancer, AIDS, and CODID-19.

In general, the level of Se concentration in a biogeochemical food chain is related to the incidence of endemic Se-deficiency pathologies. A notable role in decreasing the ecological status of Se in the biosphere is played by industrial technologies. In particular, the intense application of phosphorus-bearing fertilizers and exhaustive cropping decrease the uptake of this trace element by plants (Ermakov, 2012; Golubkina et al., 2017). A Se-deficient state is aggravated by excess As and heavy metals (which are Se antagonists), which are brought to the landscapes when deposits of base metals are developed and when other industrial processes operate (Ermakov and Jovanovic, 2010a; Bigaliev, 2018; Radosavljević et al., 2018). As a soil becomes more acidic, its quality changes, and this increases the mobility of the ions of heavy metals and aluminum. This, in turn, increases the leaching rates of heavy metals from the soil and their uptake by the networks of plant roots. The intensity of the uptake of heavy metals by plants depends not only on concentrations of the metals in the soil but also on interactions between these ions with the ions of other metals. An increase in soil acidity increases the mobility and activates the migration of trace elements in the soils and acidifies the natural waters (Moiseenko, 2009).

These processes result in the degradation of the nutritional benefits of, first, the agricultures and them the foodstuff, which leads to that the food chains contain progressively less biologically important elements.

Environmental degradation and protein and vitamin deficiencies in the human food rations, as well as a deficiency in major and trace elements in the foodstuff, result in a decrease in the Se status and a simultaneous general weakening of the immune resistance (Keen and Gershwin, 1990).

The role of food supplements in preventing diseases and their curing is obvious. Reportedly (Montagnier, 1999), AIDS is characterized by a systematic redox misbalance and a decrease in the level of glutathione concentration in the blood of the patients, which even further strengthens the oxidation stress. This researcher believes that antioxidants are valuable for suppressing the replication of the virus and the apoptosis of AIDS patients.

Selenium-deficient states are corrected and immunity is strengthened by applying various selenium-bearing compounds in pharmaceuticals with multivitamins and nutritional supplements ( Fig. 3 ). The most efficient one is Na selenite, although it is obviously toxic (Galochkin and Galochkina, 2011). Sodium selenite can oxidize SH groups in the disulfide isomerase of the virus protein, which disables the virus from passing through healthy cell membranes (Kieliszek and Lipinski, 2020). The therapy of virus-induced pathologies also utilizes other antioxidants (vitamin E, quercetin, rosemary acid, and luteolin) in combinations with antiviral, antibacterial, and immunomodulatory remedies (Krylova et al., 2016; Magagnoli at al., 2020; Zhang, lie, 2020; Zhang et al., 2020; Yao et al., 2020).

Correction technologies for selenodeficiency (Ermakov et al., 2018).

COVID-19 in Russia and the Selenium Status

Relationships between the viral pandemic disease and the Se status were estimated using information on the COVID-19 incidence in Russia over the period of time starting on September 5, 2020 ( Corona Virus, 2020) through January 29, 2021 ( Corona Virus, 2021). The scored estimation of the ecological status of various areas in Russia was carried out in compliance with a routine that had been worked out previously (Ermakov, 2001), with regard to Se concentrations in the herbaceous plants (cuts), surface- and groundwaters, annual precipitation, and the incidence of white-muscle disease in the farm livestock. The scores varied between the areas from 9 to 40 units. In addition, COVID-19 incidence was compared to the average Se concentration in the blood serum of humans in Russia, according to data available at that time (Golubkina et al., 2017; Golubkina and Papazyan, 2006).

The number sequences characterized 52 administrative units of Russia. The results obtained on relationships between COVID-19 incidence as of September 5, 2021, were processed with MS-Excel 2013 and revealed a weak negative correlation between the pathologies incidence and the Se status of the areas. The correlation coefficient between the COVID-19 incidence in Russia and the Se status was –0.362. Therewith no correlation was identified between the COVID-19 incidence and Se concentration in blood serum ( r = +0.049).

Comparison of the incidence in 52 administrative units of Russia as of January 29, 2021 ( Corona Virus, 2021), and the Se status of the territories led us to reveal a fairly strong negative correlation ( r = –0.726). However, the COVID-19 incidence (incidence per 1000 persons in Russia) and the average Se concentration in the blood serum showed a weak correlation ( r  = –0.344) ( Fig. 4 ). The correlation between the incidence and Se concentration in the grain is also weak ( r = –0.165) (Golubkina et al., 2017).

Variations in (a) COVID-19 incidence in Russia, (b) average Se concentration in human blood, and (c) scored estimates of the Se status between administrative units of Russia. (1) Moscow oblast; (2) Nizhnii Novgorod oblast; (3) Sverdlovsk oblast; (4) Rostov oblast; (5) Voronezh oblast; (6) Krasnoyarsk krai; (7) Arkhangelsk oblast; 8. Irkutsk oblast; (9) Khabarovsk krai; (10) Chelyabinsk oblast; (11) Vologda oblast; (12) Murmansk oblast; (13) Saratov oblast; (14) Stavropol krai; (15) Samara oblast; (16) Perm krai; (17) Altai krai; (18) Omsk oblast; (19) Primorie krai (Russian Southern Far East); (20) Republic Karelia; (21) Transbaikalian krai; (22) Orenburg oblast; (23) Krasnodar krai; (24) Vologda oblast; (25) Penza oblast; (26) Kirov oblast; (27) Novosibirsk oblast; (28) Leningrad oblast; (29) Republic Buryatia; (30) Kemerovo oblast; (31) Pskov oblast; (32) Bryansk oblast; (33) Tver oblast; (34) Tula oblast; (35) Tyumen oblast; (36) Yaroslavl oblast; (37) Belgorod oblast; (38) Ivanovo oblast; (39) Kaluga oblast; (40) Astrakhan oblast; (41) Republic Bashkortostan; (42) Novgorod oblast; (43) Vladimir oblast; (44) Smolensk oblast; (45) Ryazan oblast; (46) Republic Chuvashia; (47) Kabardino–Balkarian Republic; (48) Kostroma oblast; (49) Republic Tatarstan; (50) Kurgan oblast; (51) Republic of North Ossetia–Alania; (52) Republic of Marij El.

The absence of correlation between the incidence of virus pathology and Se concentration in the blood serum is likely explained by that Se concentration in the blood of humans and animals varies depending on the food status of the microelement. The status of Se, an integral parameter reflecting the level of Se concentration in the environment, is more conservative. It corresponds to a greater part of daily Se consumption, which depends on Se concentration in the environment (local agricultural foodstuff and water). In this situation, the status of Se is affected by its uncontrolled introduction into the human organism with foodstuff brought from other areas and states. Nevertheless, the variations in the Se status are smaller than the concentration of this microelement in the blood.

It should be mentioned that Se status can broadly vary within administrative units. Territories with relatively normal Se concentrations may include local areas with either very low or elevated concentrations of this element in the biogeochemical food chains. This situation is typical of Krasnoyarsk krai, Chelyabinsk oblast, Khabarovsk krai, Karelia, and Tuva (Ermakov and Kovalsky, 1974; Ermakov and Jovanovic, 2010; Golubkina et al., 2017).

The likely reasons for the difference between our estimates of relations between viral pathologies and the Se status in 2020 and 2021 are the character of the spread of this disease and the increase in the incidence in 2021.

It is pertinent to mention that relations between the incidence and Se status are better to estimate using the known biogeochemical indicator of the concentration of the microelement in the hair-covering of animals and humans. This indicator was employed by Chinese researchers (Zhang et al., 2020), and the biomaterial was obtained immediately from diseased patients. Note that in the diagnosis of Se-microelementosis in farm animals this method has proved successful (Ermakov and Usenko, 2004). However, the application of this approach for the identification of Se insufficiency in human organisms is limited by the scarcity of the data.

Zinc and Viruses

Zinc modulates antiviral and antibacterial immunity and affects inflammatory responses in the organisms of humans and animals. In spite of the absence of data of extensive clinical studies, information is currently available that a modulation of the Zn status can be important at COVID-19. For example, in vitro experiments have demonstrated that Zn 2+ shows an antiviral activity by inhibiting the RNA polymerase of SARS-CoV-2. This effect may explain the efficiency of chloroquine, which is known to be a Zn ionophore. Indirect evidence also indicates that Zn 2+ may suppress the activity of the angiotensin converting enzyme 2 (ACE2), which is a receptor for the SARS-CoV-2 virus (Rish, 2003; Chasapis et al., 2012). The enhancement of antiviral immune responses activated by Zn may result from the intensification of the synthesis of some interferon components. Thereby Zn, which is characterized by antiinflammatory activity, sometimes suppresses the development of bacterial infections. Because of its immunity-stimulating properties, Zn is used as a dietary supplement recommended at SARS.

In the context of the current pandemic induced by the COVID-19 coronavirus, Zn and Se are tested (in combinations with other pharmaceuticals, such as chloroquine and hydroxychloroquine) by some countries as a remedy against pathologies related to this disease. Scientists emphasize that a combination of Zn and a Zn-bearing transport molecule facilitates Zn penetration into cells and efficiently suppresses the replication of RNA viruses (Te Velthuis et al., 2010). Much interest is provoked by a combination of Zn compounds and flavonoids (quercetin), which seems to enhance the antioxidant action of the medicines at pathologies induced by both bacteria and viruses. However, some conclusions in this context are ambiguous (Magagnoli et al., 2020).

Biological Role of Copper

A Cu deficiency modifies the activities of several enzymes and thus induces significant disorders in the metabolic processes, for example, the exchange of lipids (a decrease in the concentrations of sphingomyelin and acetal phosphatides in the white matter of the brain and spinal cord and disorders in the myelination of the central nervous system), chromoproteides (decrease in the hemoglobin concentration, partly in relation to a retardation in erythrocyte maturation and a decrease in their lifetime), synthesis of elastin and collagen (damages of the connective tissues and ruptures of the aorta and heart vessels), distortions in the purine exchange (which may result in an increase in the activity of xanthine oxidase, synthesis of uric acid, and urate oxidase activity), and inhibition of the oxidation of most substrates of the tricarboxylic acid cycle (citrate, malate, α-ketoglutarate, pyruvate, and others) (Kovalsky, 1977; Ermakov et al., 2018).

The depression of the function of oxidizing enzymes at a Cu deficiency brings about disorders in many metabolic processes. The animal organism becomes involved in the vicious circle of interrelated reactions, and this results in the endemic diseases of ataxia in sheep (first of all, newborn lamb), cattle, and buffalo. Thereby voids develop in the brain and spinal cord because of the weakening of the synthesis of sphingomyelin and acetal phosphatides, as well as because of the depression of oxidation processes and lower oxidation of the sulfhydryl groups of neurokeratin into disulfide ones, which opens access to the proteolytic enzymes of tissues.

The newborn lambs are thereby affected by severe irreversible morphological changes in the nervous system: the cerebral hemispheres are strained, the cerebral gyri are smoothed off, the white matter of the brain swells up, and voids develop in it. Brain vessels become damaged: the permeability of the vascular walls is distorted, and vascular stasis and dystonia develop. This can also lead to the development of voids and brain edema, which affects the tissue respiration. Coupled injuries impact the motorial and sensitive pathways. Histological examinations of the peripheral nervous system have discovered dystrophic and neurobiological changes in spinal ganglions, peripheral nerve stems, and their branches in muscles. Disorders in Cu metabolism and oxidative processes in tissues of the nervous system and pathological–morphological changes in them are reflected in the clinical symptoms of ataxia: the hindquarters of the lambs are unstable at standing, their movements are discoordinated at walking, and they are affected by convulsions and paralysis (Gireev, 1968).

Copper homeostasis is regulated by a complicated system of Cu chaperone proteins. Copper deficiency is the pre-eminent disordering of the synthesis of oxidizing enzymes. Because of this, the pathologic process involves many metabolic process, and the whole organism is impacted by the disease. The epidemic disease affects 1–27% (46% at a maximum) of the sheep stock, and the mortality amounts to 70–80% of the diseased animals. However, introduction of Cu salts into the animal organisms is able to prevent the further progress of the disease (Anke et al., 1996).

At the same time, some pathologies in animals are caused by Cu excess in the forage and environment (Bath, 1979). These are various forms of so-called copper hepatitis (enzootic hepatitis). At a Cu excess, this element is accumulated in the liver with the subsequent sudden erythrocytoschisis and a sudden increase in the bilirubin concentration. The disease is of chronic nature and is characterized by a high sudden mortality rate, pancreatitis, anemia, hemoglobinia, gemoglobinuria, methemoglobinia, and deep kidney pigmentation. The Cu concentration in the nonsurviving animals is as high as 700 μg/g. An effective prophylactic remedy is Mo salts (Rish, 2001; Harr et al., 2002). Copper compounds in high concentrations are also toxic for some aquatic organisms, both plants and animals (Moiseenko, 2009).

The reasons for copper toxicity at its excess in the ration are liver functional disorders, neurodegenerative changes, and other pathological conditions. It can occur at distortions in Cu homeostasis. The ability of initiating oxidation damage is reportedly related to Cu-induced cellular toxicity. The toxicity of Cu is thought to be associated with disorders in the lipid exchange, expression of genes, the aggregation of alpha-synuclein, activation of acid sphingomyelinase and release of ceramide, and changes in the spatial distribution of Cu in hepatocytes and the proteins of the nerve glia (Gaetke et al., 2014).

Copper significantly competitively affects Fe and Mo metabolism. Along with Zn, Cu is involved in the superoxide dismutase enzyme and thus participates in blocking excess highly toxic oxygen radicals, which are formed at metabolism of various products. Superoxide dismutase (SOD, EC 1.15.1.1) affiliates with the group of antioxidative enzymes. It catalyzes superoxide dismutation into oxygen and hydrogen peroxide and also precludes the oxidation of some biologically active substances (Ermakov et al., 2016). The identification of SOD activity in the blood of animals and humans is important when several pathologies are encountered. Thereby an important role in the SOD activity is played by Cu and Zn.

Antimicrobial and Antiviral Properties of Copper

Antimicrobial properties of Cu have been known to the humankind since high antiquity. Copper sulfate turned out to be an efficient fungicide and was used in the preservation treatment of wood for construction purposes. Copperware was also found out to show bactericide properties. Copper drinking cups were manufactured and utilized in ancient India, and copperware is still customarily widely utilized in this country. Most water piping in the United States is made up of copper and copper alloys. Copper started to be widely applied in the construction industry with the beginning of the industrial revolution in the late 19th century. The metal is widely applied in the fitting and decoration of interiors. In the 20th century, this metal gradually gave way first to stainless steel and quenched glass and then also to plastics.

It is currently known that Cu compounds and nanoparticles are efficient in fighting bacteria and viruses. For example, experiments by Ph.J. Kuhn in 1983 have demonstrated that Cu is able to decontaminate the surfaces of various Cu-bearing articles (Kuhn, 1983). Together with her students, this researcher carried out experiments on tamponing door knobs and handles, as well as other items made up of various materials. After the experiments, the cotton tampons were placed into Petri dishes, and then (in a few days) microflora in them was studied. The copper surfaces turned out to be much cleaner than the steel and plastic ones. Based on the results of the experiments, these researchers recommended not to rid of copper items or substitute them for analogous ones made of other materials.

The efficiency of Cu and its alloys as antimicrobial coatings have been estimated by the invasion of aurococcus Staphylococcus aureus . Again, the aluminum and steel surfaces were coated with a micrometer-thick Cu layer (applied by means of plasma, electric-arc, or cold sputter coating). Upon the sterilization of the prepared platelets, suspension with aurococcus from infected patients was applied to these platelets (after the sterilization of the prepared platelets). Aliquots of washoffs from the platelets (made in 2 h) were then placed into a Petri dish, and the staphylococcus colonies were led to grow (Champagne and Helfritch, 2013). The technique of cold sputtering has proved to be mostly antimicrobial because of the high activities of the sputtered particles at their collisions, which resulted in a high density of dislocation and intense ion diffusion ( Fig. 7 ).

Survival of Staphylococcus aureus on Al-disk with Cu-spraying after treatment for 2 h exposure. The processing methods are: (a) laser sputter coating, (b) electric-arc sputtering, (c) cold spraying (Champagnie and Heifritch, 2013).

A.A. Rakhmetova (2011) has found out that the antimicrobial action of Cu nanoparticles depends on their content: when used in a concentration of 1 to 10 μg/L, Cu nanoparticles of sample 1 have shown a bactericidal action, they acted bacteriostatically when in a concentration of 0.5 μg/L, and no antimicrobial effect was identified when the concentration was 0.1 μg/L.

The spectrum of Cu action on microorganisms is very wide. Results of independent experiments conducted at laboratories of the United States Environmental Protection Agency in compliance with approved EPA protocols have proved that more that 99.9% bacteria die on copper, brass, and bronze surfaces within 2 h. These bacteria are

• aurococcus ( Staphylococcus aureus ),

• aerobacter ( Enterobacter aerogenes ),

• coliform bacillus ( Escherichia coli ),

• blue pus bacillus ( Pseudomonas aeruginosa ),

• listeria monocytogene ( Listeria monocytogenes ),

• vancomycin-tolerant enterococcus ( Enterococcus faecalis (VRE)),

• vancomycin- and methicillin-resistant aurococcus (meticillin-resistant Staphylococcus aureus (MRSA)),

• Clostridium difficile ,

• salmonella (bacillus Gartner, Salmonella enteriditis )

• tubercle bacillus ( Tubercle bacillus ),

• acinetobacter Baumannii ( Acinetobacter baumannii ).

Moreover, Cu has been demonstrated to be able to kill adenovirus, Candida fungus ( Candida albicans ), black mold ( Aspergillus niger ), grippe A virus, and poliovirus. No other materials, even silver-bearing, are equally efficient. According to other researchers, Cu nanoparticles more obviously than Fe nanoparticles can inhibit of the growth of clinical isolates of aurococcus. The degree of inhibition also depends on the dozes of the ultrafine powders and on the incubation time (Babushkina et al., 2010; Molteni et al., 2010; Lemire et al., 2013; Warnes, 2014).

The surfaces of antimicrobial brass and bronze were characterized by a long-lasting antibacterial effect, which did not weaken within 2 h and killed the overwhelming majority of the bacteria even after wet and/or dry wiping and subsequent recontamination.

Although the mechanism by which Cu kills bacteria is complicated, its effect is simple. The effect of copper surfaces on bacteria is thought to involve two successive phases. First, a copper surface interacts with the outer membrane of the organism and thus damages the membrane of the pathogen. During the second phase, the microorganism cell looses water and nutrients through these holes in its membrane. A certain role in the inactivation of the microorganisms is therewith played by the transmembrane potential of the cell (Wobus et al., 2006; Griffith, 2012).

Decades after the first viral pandemic diseases spread, scientists estimated in much detail the role of Cu in deactivation of various viruses, including coronavirus 229E (a precursor of COVID-19) and COVID-19 itself (Warnes et al., 2015). A research team headed by William Keevil has proposed to apply Cu to fight coronavirus, with copper elements applied as widely as possible in public places. It is expedient to use this metal in manufacturing door knobs and handles, stair railings, and hand-rails in buses, trains, and other public transport. Thereby COVID-19 is deactivated in copper surfaces within a few hours by Cu ions, which attack the lipid membrane of the virus, invade it, and destroy its nucleic acids (Warnes et al., 2015).

Along with copper materials, nanocopper is nowadays progressively more widely used as an antiviral remedy (Frolov, 2020). A research team headed by G. Frolov at the National University of Science and Technology MISiS have synthesized the new Cu-based medicine spirtozol for the surface treatment of individual protective equipment, clothes, and various surfaces. This healthcare products is suspension of Cu nanoparticles (1 to 3 nm) in ethanol solution of the antiseptic cetyl pyridinium chloride. At disinfection treatment in wet air, Cu is transformed on the surface into positively charged ions of Cu hydroxide, which ensures the desired protection of the treated items against viruses and other pathogens. In this situation, Cu hydroxide ions are “soft” electrophilic agent, which enters a chemical reaction with sulfur-bearing structures of the virus and modifies the pH of the medium (acidifies it). This damages the envelope of any organism, including a virion. However, this medication in high concentrations is also hazardous for the cells of the host organism and may leads to irritation of its skin integuments. Healthcare products based on copper ions and copper compounds were proposed for usage as severe external disinfectants when applied together with the antiseptic cetyl pyridinium chloride (Frolov, 2020).

Biological Importance of Iodine

Upon coming with food into the gastrointestinal system, iodine compounds are reduced to iodides and are absorbed mostly in the small intestine. The absorbed iodine is spread by blood throughout the organism, and its excess is deposited in lipids. It is mostly (up to 60%) absorbed by the thyroid gland and is then used to synthesize hormones. In the thyroid gland, blood iodides release free metalloid iodine under the effect of the enzyme iodidase. The molecular iodine is bound with the aminoacid tyrosine to form mono- and diiodotyrosine, from which thyroid hormones are synthesized: triiodothyronine (Т 3 ) and tetraiodothyronine (Т 4 ). These hormones are brought to blood to be bound in it with the globulins and albumines of the plasma. Iodine-bearing thyroid hormones stimulate the synthesis of many enzymes, increase their activity, and are thus involved in regulation of the metabolic activity and various physiological processes and functions (Rish, 2001; Ermakov et al., 2018).

Iodine participates in the development and differentiation of tissues, enhances oxygen absorption by tissues, and increases its utilization coefficient. This element activates heat production, synthesis of proteins in cells, and increases the activity and concentrations of cyclic 3,5-adenosine monophosphate in cells. Iodine stimulates trophic and immune processes, erythropoiesis, leucopoesis, the secretory activity of the digestive and lacteal glands, the synthesis of milk fat, the activity of the generative organ, and fetation (Rish, 2003).

An iodine deficiency in the organisms of mammals is thought to be responsible for iodine-deficiency pathologies. One of the most widespread of them is endemic hypothyroidism. Nevertheless, the endocrinous function of iodine is interrelated with selenium (see above). Because of this, both of the trace elements are interrelated in metabolic and pathophysiological processes. Pathologies triggered by excess iodine are rare and are mostly allergic reactions, such as erubescence, breathlessness, etc. (Andryukov et al., 2015).

It is known that iodine was applied in the course of prophylaxis and therapy during the pandemic of COVID-19. The unique bactericide properties of iodine have been known for a long time (Kelly, 1961). Treatment with Mandla paint (tretman) in the course of 1957 Asian flue pandemic prevented the development of the disease. The percentage of diseased persons in the group to which no tretman was administered amounted to 14%, and that in the group treated with this medicine was 2.8%. Moreover, treatment with iodine even when flue was already in progress significantly decreased (after 3 days) the disease incidence compared to that in the control group, with the effect manifesting itself in 2 days after tretman was first administered (Menon, 1957).

Pathophysiological studies demonstrate that iodine can support the congenital immune system in fighting bacterial and viral infections (Fischer et al., 2011; Derscheid et al., 2014). In 2013, it has been demonstrated that iodine treatment of newborn lambs infected by respiratory syncytial virus (RSV) resulted in smaller damages of the lungs and smaller expression of RSV antigen in the lungs. It has also been demonstrated that administering iodine to three-week old lambs makes their RSV infection less severe (Derscheid et al., 2014). Finally, epidemiological data show that the current COVID-19 pandemic in the Japanese, who are known to consume much iodine, resulted in a very low COVID-19 mortality rate compared to other nations, in spite of the facts that the population of Japan is the world’s oldest and that the national isolation policy was so far relatively soft ( WHO, 2019).

The aforementioned pathophysiological, clinical, and epidemiological data suggest that iodine may be a crucially important trace element for the optimal functioning of the immune system and can be efficient in fighting the COVID-19 pandemic, both clinically and preventively. Its prevention can be readily reached thanks to the very limited adverse side reactions and because of the fast uptake of the medicines when administered per orally. Also, it is worth mentioning in this context that one-third of the world’s population currently suffers from iodine deficiency (Verheesen and Traksel, 2020).

CONCLUSIONS

This publication presents a review of one of the phases of the current state of the biosphere: its anthropogenic modification and progressively more aggravating ecological problems. In spite of the undeniable advances in genetics, molecular biology, and virology, the humankind is impacted by unpredictable diseases: severe viral pathologies.

From the ecological standpoint, these problems once again highlight the unity and complicatedness of relations between discrete groups of living organisms and life cofactors. The COVID-19 viral pandemic is viewed by scientists as one of the stages of the variability of RNA-bearing viruses as a consequence of a combination of the anthropogenically affected evolution of the environment and disturbances in the links established between various organisms. Following ecological genetics, ecological virology starts developing. This is science that centers on interrelations between the host and virus. Mechanisms underlying these interactions are complicated and still poorly understood. However, the role of geochemical factors, as well as other features of the habitats of organisms, is thereby particularly important.

Relations between viral infections and biogeochemical factors once again confirms the validity of one of the concepts of geochemical ecology: the law of a minimum. On the one hand, the geochemical factor (in this situation, this is the status of necessary chemical elements) highlights life interrelations between organisms at a deficiency of elements. On the other hand, this also pertains to situations with an excess in trace elements in a biogeochemical food chain. For example, a Se deficiency makes humans more vulnerable to RNA-viral infections, with more severe disease outcomes. However, excess Se in the habitat leads to toxicosis in human and animal organisms and weakens their immunity.

Such relations are typical not only of Se but also of other vitally important trace elements, such as Zn, Cu, I, and Co. However, toxic properties of metals can be utilized in designing antibacterial and antiviral technologies, as was demonstrated at interaction of viruses and bacteria with the surface of copper items, nanoparticles of the metal, and its solute species.

The aforementioned facts of the participation of trace elements in strengthening immunity, as in the prevention of cancer and some other hazardous viral diseases (hepatitis, Ebola hemorrhagic fever, and COVID-19), highlight still other aspects of the biological role of trace elements. Similar to Se, Zn, Cu, and I are utilized in the prophylaxis of cardiovascular diseases and are involved in regulating the reproductive function and the functioning of the thyroid gland, as well as in preventing cataract and other diseases. This brings forth the key role played by vitally important trace elements in maintaining the health of human populations.

However, although much is known already on relations between deficiencies in trace elements and viral infections, this issue calls for further deeper virological, biochemical, and epidemiological studies. Nowadays the beneficial effects of trace-element food supplements can be viewed as therapeutic.

Moreover, current complicated geochemical states and conditions make it necessary to evaluate the criterion integral statuses of trace elements.

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Ermakov, V.V., Jovanović, L.N. Biological Role of Trace Elements and Viral Pathologies. Geochem. Int. 60 , 137–153 (2022). https://doi.org/10.1134/S0016702922020045

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March 13, 2024

Scientists reveal the first unconventional superconductor that can be found in mineral form in nature

Scientists from Ames National Laboratory have identified the first unconventional superconductor with a chemical composition also found in nature. Miassite is one of only four minerals found in nature that act as a superconductor when grown in the lab. The team’s investigation of miassite revealed that it is an unconventional superconductor with properties similar to high-temperature superconductors. Thier findings further scientists’ understanding of this type of superconductivity, which could lead to more sustainable and economical superconductor-based technology in the future.

Superconductivity is when a material can conduct electricity without energy loss. Superconductors have applications including medical MRI machines, power cables, and quantum computers. Conventional superconductors are well understood but have low critical temperatures. The critical temperature is the highest temperature at which a material acts as a superconductor.

In the 1980s, scientists discovered unconventional superconductors, many of which have much higher critical temperatures. According to Ruslan Prozorov, a scientist at Ames Lab, all these materials are grown in the lab. This fact has led to the general belief that unconventional superconductivity is not a natural phenomenon.

Prozorov explained that it is difficult to find superconductors in nature because most superconducting elements and compounds are metals and tend to react with other elements, like oxygen. He said that miassite (Rh 17 S 15 ) is an interesting mineral for several reasons, one of which is its complex chemical formula. “Intuitively, you think that this is something which is produced deliberately during a focused search, and it cannot possibly exist in nature,” said Prozorov, “But it turns out it does.”

Paul Canfield, Distinguished Professor of Physics and Astronomy at Iowa State University and a scientist at Ames Lab, has expertise in design, discovery, growth, and characterization of novel crystalline materials. He synthesized high quality miassite crystals for this project. “Although miassite is a mineral that was discovered near the Miass River in Chelyabinsk Oblast, Russia,” said Canfield, “it is a rare one that generally does not grow as well-formed crystals.”

Growing the miassite crystals was part of a larger effort to discover compounds that combine very high melting elements (like Rh) and volatile elements (like S). “Contrary to the nature of the pure elements, we have been mastering the use of mixtures of these elements that allow for low temperature growth of crystals with minimal vapor pressure,” said Canfield. “It’s like finding a hidden fishing hole that is full of big fat fish. In the Rh-S system we discovered three new superconductors. And, through Ruslan’s detailed measurements, we discovered that the miassite is an unconventional superconductor.”

Prozorov’s group specializes in advanced techniques to study superconductors at low temperatures. He said the material needed to be as cold as 50 millikelvins, which is about -460 degrees Fahrenheit.

Prozorov’s team used three different tests to determine the nature of miassite’s superconductivity. The main test is called the “London penetration depth.” It determines how far a weak magnetic field can penetrate the superconductor bulk from the surface. In a conventional superconductor, this length is basically constant at low temperature. However, in unconventional superconductors, it varies linearly with the temperature. This test showed that miassite behaves as an unconventional superconductor.

Another test the team performed was introducing defects into the material. Prozorov said that this test is a signature technique his team has employed over the past decade. It involves bombarding the material with high-energy electrons. This process knocks-out ions from their positions, thus creating defects in the crystal structure. This disorder can cause changes in the material’s critical temperature.

Conventional superconductors are not sensitive to non-magnetic disorder, so this test would show no or very little change in the critical temperature. Unconventional superconductors have a high sensitivity to disorder, and introducing defects changes or suppresses the critical temperature. It also affects the critical magnetic field of the material. In miassite, the team found that both the critical temperature and the critical magnetic field behaved as predicted in unconventional superconductors.

Investigating unconventional superconductors improves scientists understanding of how they work. Prozorov explained that this is important because, “Uncovering the mechanisms behind unconventional superconductivity is key to economically sound applications of superconductors.”

This research is further discussed in “ Nodal superconductivity in miassite Rh 17 S 15 ,”written by, Hyunsoo Kim, Makariy A. Tanatar, Marcin Kończykowski, Romain Grasset, Udhara S. Kaluarachchi, Serafim Teknowijoyo, Kyuil Cho, Aashish Sapkota, John M. Wilde, Matthew J. Krogstad, Sergey L. Bud’ko, Philip M. R. Brydon, Paul C. Canfield, and Ruslan Prozorov, and published in Communications Materials.

This work was supported by the DOE Office of Science (Office of Basic Energy Sciences) and used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility.

Ames National Laboratory is a U.S. Department of Energy Office of Science National Laboratory operated by Iowa State University. Ames Laboratory creates innovative materials, technologies, and energy solutions. We use our expertise, unique capabilities, and interdisciplinary collaborations to solve global problems.

Ames Laboratory is supported by the Office of Science of the U.S. Department of Energy. The Office of Science is the single largest supporter of basic research in the physical sciences in the United States and is working to address some of the most pressing challenges of our time. For more information, please visit https://energy.gov/science .

Scientists reveal the first unconventional superconductor that can be found in mineral form in nature

Scientists from Ames National Laboratory have identified the first unconventional superconductor with a chemical composition also found in nature. Miassite is one of only four minerals found in nature that act as a superconductor when grown in the lab. The team's investigation of miassite revealed that it is an unconventional superconductor with properties similar to high-temperature superconductors. Their findings further scientists' understanding of this type of superconductivity, which could lead to more sustainable and economical superconductor-based technology in the future.

Superconductivity is when a material can conduct electricity without energy loss. Superconductors have applications including medical MRI machines, power cables, and quantum computers. Conventional superconductors are well understood but have low critical temperatures. The critical temperature is the highest temperature at which a material acts as a superconductor.

In the 1980s, scientists discovered unconventional superconductors, many of which have much higher critical temperatures. According to Ruslan Prozorov, a scientist at Ames Lab, all these materials are grown in the lab. This fact has led to the general belief that unconventional superconductivity is not a natural phenomenon.

Prozorov explained that it is difficult to find superconductors in nature because most superconducting elements and compounds are metals and tend to react with other elements, like oxygen. He said that miassite (Rh 17 S 15 ) is an interesting mineral for several reasons, one of which is its complex chemical formula. "Intuitively, you think that this is something which is produced deliberately during a focused search, and it cannot possibly exist in nature," said Prozorov, "But it turns out it does."

Paul Canfield, Distinguished Professor of Physics and Astronomy at Iowa State University and a scientist at Ames Lab, has expertise in design, discovery, growth, and characterization of novel crystalline materials. He synthesized high quality miassite crystals for this project. "Although miassite is a mineral that was discovered near the Miass River in Chelyabinsk Oblast, Russia," said Canfield, "it is a rare one that generally does not grow as well-formed crystals."

Growing the miassite crystals was part of a larger effort to discover compounds that combine very high melting elements (like Rh) and volatile elements (like S). "Contrary to the nature of the pure elements, we have been mastering the use of mixtures of these elements that allow for low temperature growth of crystals with minimal vapor pressure," said Canfield. "It's like finding a hidden fishing hole that is full of big fat fish. In the Rh-S system we discovered three new superconductors. And, through Ruslan's detailed measurements, we discovered that the miassite is an unconventional superconductor."

Prozorov's group specializes in advanced techniques to study superconductors at low temperatures. He said the material needed to be as cold as 50 millikelvins, which is about -460 degrees Fahrenheit.

Prozorov's team used three different tests to determine the nature of miassite's superconductivity. The main test is called the "London penetration depth." It determines how far a weak magnetic field can penetrate the superconductor bulk from the surface. In a conventional superconductor, this length is basically constant at low temperature. However, in unconventional superconductors, it varies linearly with the temperature. This test showed that miassite behaves as an unconventional superconductor.

Another test the team performed was introducing defects into the material. Prozorov said that this test is a signature technique his team has employed over the past decade. It involves bombarding the material with high-energy electrons. This process knocks-out ions from their positions, thus creating defects in the crystal structure. This disorder can cause changes in the material's critical temperature.

Conventional superconductors are not sensitive to non-magnetic disorder, so this test would show no or very little change in the critical temperature. Unconventional superconductors have a high sensitivity to disorder, and introducing defects changes or suppresses the critical temperature. It also affects the critical magnetic field of the material. In miassite, the team found that both the critical temperature and the critical magnetic field behaved as predicted in unconventional superconductors.

Investigating unconventional superconductors improves scientists understanding of how they work. Prozorov explained that this is important because, "Uncovering the mechanisms behind unconventional superconductivity is key to economically sound applications of superconductors."

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Materials provided by DOE/Ames National Laboratory . Note: Content may be edited for style and length.

Journal Reference :

• Hyunsoo Kim, Makariy A. Tanatar, Marcin Kończykowski, Romain Grasset, Udhara S. Kaluarachchi, Serafim Teknowijoyo, Kyuil Cho, Aashish Sapkota, John M. Wilde, Matthew J. Krogstad, Sergey L. Bud’ko, Philip M. R. Brydon, Paul C. Canfield, Ruslan Prozorov. Nodal superconductivity in miassite Rh17S15 . Communications Materials , 2024; 5 (1) DOI: 10.1038/s43246-024-00456-w

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• Published: 11 June 2018

Environmental legacy contributes to the resilience of methane consumption in a laboratory microcosm system

• Sascha M. B. Krause 1 , 2 ,
• Marion Meima-Franke 2 ,
• Annelies J. Veraart   ORCID: orcid.org/0000-0001-6286-7484 2 , 3 ,
• Gaidi Ren 4 , 5 ,
• Adrian Ho 2 , 6 &
• Paul L. E. Bodelier 2  

Scientific Reports volume  8 , Article number:  8862 ( 2018 ) Cite this article

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• Microbial ecology

The increase of extreme drought and precipitation events due to climate change will alter microbial processes. Perturbation experiments demonstrated that microbes are sensitive to environmental alterations. However, only little is known on the legacy effects in microbial systems. Here, we designed a laboratory microcosm experiment using aerobic methane-consuming communities as a model system to test basic principles of microbial resilience and the role of changes in biomass and the presence of non-methanotrophic microbes in this process. We focused on enrichments from soil, sediment, and water reflecting communities with different legacy with respect to exposure to drought. Recovery rates, a recently proposed early warning indicator of a critical transition, were utilized as a measure to detect resilience loss of methane consumption during a series of dry/wet cycle perturbations. We observed a slowed recovery of enrichments originating from water samples, which suggests that the community’s legacy with a perturbation is a contributing factor for the resilience of microbial functioning.

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Introduction.

Microbial communities are crucial components of every ecosystem, and are important drivers of global biogeochemistry 1 . Their significance is now widely established with an increased interest to understand the world’s microbiomes 2 , 3 . A pressing research question is the quantification and prediction of the response of microbial processes to the increase of extreme weather phenomena as well as human impacts on natural systems.

Environmental history has been identified as an determining factor for current microbial communities and functioning 4 , 5 . In so-called legacy effects, past biotic and abiotic conditions persist through time even if the environment is altered, which affects the response to changing environmental conditions in present microbial communities 6 , 7 . Therefore, it is reasonable to assume that microbial communities from environments without prior exposure to a specific change in environmental conditions may only have limited capacity to respond to such a perturbation 8 .

Resilience is a way to quantify such responses and is broadly defined into engineering resilience, which simply refers to the recovery over time, and ecological resilience, which measures the amount of disturbance necessary to move a system to an alternative stable state 9 . Both processes are connected in the concept of critical slowing down that has been introduced to biology only recently 10 . It suggests that the rate of recovery from multiple small scale disturbances (i.e. engineering resilience) can be used as a measure to a tipping point in biological systems at which the system switches into another stable state (i.e. ecological resilience) 10 , 11 . Note that slowed recovery is not only a sign of an impending catastrophic shift, but can also signal potential decreasing stability in systems without alternative stable states 12 , whereas rapid regime shifts and chaotic bifurcations can also occur without slowing of recovery rates 13 , 14 .

The existence of this novel indicator in biological systems has been shown in previous studies. For instance, Dakos and Bascompte 15 detected indications for critical slowing down using the structure of 79 mutualistic networks from ecological communities. In another study Veraart and colleagues 16 used cyanobacteria as an example to demonstrate critical slowing down before an induced transition to a tipping point. Hence, slowed recovery may represent a suitable indicator with great promises to rank the response to perturbation of complex microbial systems.

However, measuring specific microbial responses in complex environmental communities is still a challenging task. Alternatively, laboratory model systems represent a simplified approach that enables controlled manipulations and detailed analysis of individual species responses and feedbacks.

Aerobic methane-oxidizing bacteria (methanotrophs) are a key microbial group that catalyzes the degradation of a major greenhouse gas and is thus of great importance for the global climate and methane budget 17 , 18 . Previous studies using methanotrophs demonstrated a high recovery rate from experimental disturbances such as dry-wet cycles 8 , desiccation and heat stress 19 , nitrogen pulse at different methane source strengths 20 , and have been shown to recolonize disturbed habitats 21 suggesting that these organisms have a high capacity to survive and persist a range of environmental conditions. In addition, laboratory microcosms and field experiments using stable isotope probing techniques have shown that in the presence of methane as main carbon source, co-occurring non-methanotrophic communities are not random 22 , 23 , allowing to reduce the total microbial community to functionally relevant, potentially interacting non-methanotrophic taxa. Hence, aerobic methane consumption represents an ideal model system to study basic principles of microbial resilience with a defined subset of interacting microbial communities.

In this study, we hypothesized that the functionally relevant methanotrophic communities originating from soil (always dry), sediment (periodic dry) and water (never dry), i.e. different legacies in exposure to dry-wet cycles, would become increasingly vulnerable to perturbations due to loss of “ecological resilience”. To test whether biomass (expressed as abundance) and changes in the total non-methanotrophic community by the perturbations are the driver underlying a loss of resilience, we designed a laboratory microcosm setup using diluted and undiluted enrichments of methanotrophs and the associated total microbial community. We focused on recovery as an indicator that can be used to detect resilience loss in important microbial ecosystem processes.

Methane consumption rates

First, we observed that no methane consumption could be measured from any environment one day after each dry/wet cycle perturbation (Fig.  1 ). Second, most replicates from different environments resumed activity after seventeen days following the first perturbation (Fig.  1 ). After the second and third perturbation cycle, we observed a pattern in which samples from different environments resumed activity already after five days, except for the water samples (Fig.  1 ). We did not find any apparent trend with enrichments from diluted samples (Fig.  1 ).

Methane consumption rates of individual microcosm enrichments at different time points during the course of the experiment (n = 4 for each group). The first column (Ref) depicts methane consumption rates from microcosms after two weeks of pre-incubation and before the first dry/wet cycle perturbation.

Recovery of methane consumption after each dry/wet cycle perturbation

We then calculated recovery from perturbation as a metric to describe resilience loss of an important microbial process (Supplementary Information Table  S1 ). We show that the lag phase in all environments and dilutions after the first perturbation (Fig.  2a ) disappeared from the soil and sediment samples but increased in the water samples after the third perturbation (Fig.  2b ). Again, no apparent trend was observed with enrichments from diluted samples (Figs  1 and 2 ).

Normalized recovery of methane consumption rates after the first dry/wet cycle perturbation ( a ) and the third dry/wet cycle perturbation ( b ), (mean ± s.d; n  = 4 for each setup). A detailed description can be found in Material and Methods.

Community composition after a series of dry/wet cycle perturbation

We used Illumina 16S rDNA sequencing to evaluate whether changes in the total bacterial methanotrophic community structure were linked to the observed differences of resilience in methane consumption from different environments. The microbial community composition in all samples from different environments had significantly different community structures (ANOSIM R: 0.864, P  < 0.001; Fig.  3a ). We identified a separation based on environment and treatment (Fig.  3a ). We then partitioned the data set into methanotrophs and non-methanotrophs. Intriguingly, the non-methanotrophic part of the community contributed strongest to the separation of different environments (Fig.  3b ) while the methanotrophic community was more similar among samples (Fig.  3c ). An analysis of the diversity parameters richness, evenness, and Shannon index did reveal any obvious trends (Supplementary Information Table  S2 ).

Nonmetric multidimensional scaling analysis showing the community composition of the total and methanotrophic community ( a ), the fraction of non-methanotrophic bacteria ( b ), and the fraction methanotrophic bacteria ( c ) derived from the standardized 16S rDNA-based sequencing data (treated water samples n = 3, treated diluted water samples n = 2, treated and control soil samples n = 3, treated sediment samples n = 3, all remaining n = 4).

We then compared the identity of dominant taxa within methane-consuming communities from perturbated and unperturbed samples (Fig.  4 ). In particular, the family Chitinophagaceae were almost absent in perturbated enrichments originating from water samples. In addition, the families Methylophilaceae and Crenotrichaceae . displayed strong patterns in enrichments that originated from sediment samples. Members of these families were only found in perturbated samples and were below the detection limit in control samples (Fig.  4 ). Contrastingly, the family Commamonadaceae showed a higher relative abundance in controls than in perturbated samples. This was independent from the origin of samples (Fig.  4 ).

Heatmap of the 20 most abundant non-methanotrophic bacteria at the family and Phylum level derived from the standardized 16S rDNA-based sequencing data (treated water samples n = 3, treated diluted water samples n = 2, treated and control soil samples n = 3, treated sediment samples n = 3, all remaining n = 4). For this analysis standardized 16S rDNA-based sequencing data was further simplified by removing single and doubletons and focusing on sequences with a relative abundance of >1% to obtain a better visual representation. Control (C) and Treatment (T).

Abundance of total bacteria and methanotrophs during a series of dry/wet cycle perturbations

Since Illumina 16S rDNA sequencing gives only relative abundances of the present bacterial community we further evaluated temporal dynamics of total bacteria and methanotroph’s abundance using quantitative PCR (qPCR) assays (Fig.  5 ). We focused on enrichments originating from water samples because these samples depicted clear signs of slowing down in the recovery of methane consumption, which allowed evaluating whether abundance is a driver of loss in resilience. First, we confirmed that the dilution treatment decreased the overall abundance of the bacterial community based on quantitative PCR of the 16S rDNA (Fig.  5 ). We did not expect total abundance of methanotrophs to vary between dilutions since we enriched for methanotrophs (Fig.  5 ). Second, the abundance of total and methanotrophic bacteria decreased in disturbed microcosms over time (Fig.  5 ). We further observed an increase in total and methanotrophic bacteria in the diluted water samples at day 17 after the first perturbation (Fig.  4 ).

qPCR analysis of total bacteria (based 16S rDNA, a , b ) and total methanotrophic population (based on the marker gene pmoA , transcribes subunit of key enzyme in methane oxidation, c , d ) from enrichments originating water samples. The assays were performed in duplicate from each DNA extract (2 ng/μL) for each of the four replicates (mean ± s.d; n = 8) before the first dry/wet cycle perturbation, after three and 17 days of the first dry/wet cycle perturbation (>1st Pert.), and 13 days after the third dry/wet cycle perturbation (>3rd Pert.). Asterisks above the x axis indicate significance between control and treatment conditions at different time points (*** P  < 0.001; ** P  < 0.01; * P  < 0.05).

In this study, we used a microbial model system to test legacy effects as basic principle that is important in microbial resilience. We hypothesized that environmental legacy towards drought in enriched and functionally relevant methane-consuming communities originating from soil (always dry), sediment (periodic dry) and water (never dry), persists when exposed to a series of dry/wet cycle perturbations.

In accordance with our hypothesis, we demonstrate that the recovery of methane consumption in enrichments originating from the water column, with no legacy in exposure to dry/wet cycle perturbations, slowed down over time. This indicates a loss of resilience after recurring perturbations, which can prelude a collapse in the methanotrophic community 16 .

Previous work in soil has shown that methane consumption was not considerably compromised by disturbances and even displayed higher activities compared to undisturbed communities, but at the expense of community evenness 24 , 25 . Hence, one could argue that biomass and changes in community structure by the repeated perturbations are drivers underlying the loss of resilience. However, abundance dynamics of the total bacterial community in enrichments originating from water samples did not fully explain the slowed recovery but suggested a contribution of the non-methanotrophs to the recovery trend (Figs  1 and 5 ). Similarly, diversity parameters were not directly correlated to the observed differences in recovery but depicted the lowest richness in unperturbed enrichments from water samples (Supplementary Information Table  S2 ). Scheffer and colleagues 26 suggested that in highly connected (interacting) systems local perturbations can be buffered quickly through feedbacks from the system itself. In this study, soil and sediment enrichments recovered even faster after repeated dry/wet cycle perturbations, given sufficient recovery period (Fig.  2 ). High interactions between taxa of soil and sediment microbial communities could therefore underlie their fast recovery, even after repeated perturbations.

Previous work already provided direct evidence that the presence of non-methanotrophic heterotrophs resulted in increased methanotrophic activity 27 . Hence, non-methanotrophic heterotrophs may be an important component in the resilience towards perturbations. In this study, we used an experimental design, in which the methanotrophs act as a key species that support non-methanotrophic bacteria, e.g. by cross-feeding carbon from methane to other microbial species 22 , 23 , 28 . Members of the family Chitinophagaceae were linked to the dry/wet cycle perturbation in water enrichments, but their effect on methanotrophs remains speculative. Interestingly, the co-enriched members of Beta-proteobacteria were highly abundant in the total bacteria communities and showed distinct patterns between control and perturbated enrichments. Considering methanol as the first product in aerobic methane oxidation it is not surprising that the family Methylophilaceae , which includes methanol-utilizers, responded strongly. It suggests that members of the family Methylophilaceae may be involved in stabilizing methanotrophic community functioning in enrichments originating from the sediment. By co-enriching methanotrophs and non-methanotrophic bacteria the history of the original habitat may have been preserved in terms of the interacting communities. Hence, a legacy effect may arise from the non-methanotrophic bacteria present originally, co-enriched and supporting methanotrophs in a yet unknown way 29 .

In conclusion, the application of a microcosm model system demonstrates a loss of resilience in functionally relevant methanotrophic microbial communities that have never been exposed to dry-wet cycles. This suggests that legacy effects contribute to the response of microbial processes to perturbation in our study. More mechanistically, we observed an example of slowed recovery of methanotrophic communities giving new support to the existence of slowing down as an indicator before a possible collapse or loss of function. In addition, we fueled the on-going debate that microbial functions widely distributed among microbes are likely to be more redundant and therefore may be compensated by other members of the microbial community 30 in case of perturbation. Individual taxa may still have important additional functions for specialized groups such as methanotrophs and losses in their diversity will likely reduce important functions such as methane consumption.

Material and Methods

Sampling and selective pre-incubations.

Soil and water samples were collected in December 2013 from a study area in the Horstermeer polder in the Netherlands, which has previously been described 31 , 32 , 33 . Three cores (20 cm length, 3.8 cm diameter) of soil were taken at random locations with a soil corer. The water column of the ditch was sampled using a bucket and water was transferred into 500 ml jars that were closed with a lid. In addition, three sediment samples were collected in the same way as soil samples from the Polder Nootdorp in the Netherlands, an aquatic system that has been described in a previous study 34 .

Samples were transported back to the laboratory and immediately processed. From the soil and sediment, the top five centimeter were homogenized separately and 5 grams were weighed into 150 ml flasks and 20 ml of five times diluted nitrate mineral salt medium (M2) was added 35 in triplicates. Flasks were capped with grey rubber stoppers (Sigma-Aldrich, St Louis, MO, USA) and 5% (v/v) pure methane was added. The incubations were performed for one week at 20 °C in the dark on a gyratory shaker (120 rpm) to enrich for methanotrophs and reduce the complexity of the total microbial community to associated functionally relevant non-methanotrophic heterotrophs. Water samples were incubated in the same way as soil and sediment samples except that 5 ml of water were mixed with 15 ml of M2 medium.

Experimental setup and perturbations

These enrichments of methanotrophic communities from different environments were used as starting material for the main experiment. We prepared two setups to test for the effect of biomass and changes in the total non-methanotrophic community composition to explain loss of resilience. In the first setup enrichments were diluted 1:3000 and in another setup enrichments were used undiluted. For all setup microcosms were prepared that consisted of 120 ml serum bottles that were filled with 20 ml enrichment mix. Enrichment mix was prepared by mixing 20 ml enrichment with 160 ml M2 medium. Microcosms were capped with rubber stoppers (Sigma-Aldrich) and 5% (v/v) pure methane was added to the headspace. The incubations were performed for another week at 20 °C in the dark on a gyratory shaker (120 rpm) to further enrich for methanotrophic communities and to ensure that any initial effects from setting up the experiment were minimized. For each environment we prepared eight microcosms, four replicated controls and treatments, in total 52 samples. Please note that the 8 samples for diluted soil did not show any growth (turbidity) or activity (methane oxidation) before the start of the experimental perturbations and were removed from the experiment.

Three dry/wet cycle perturbations were applied during the experiment, the first after 7 days, a second after 36 days, and a third after 45 days. For each dry/wet cycle perturbation the four treatment microcosms from each environment were dried overnight using pressurized air. Please note that pre-experiments showed that these microcosms will cool down to 15 °C during this process. Therefore, control microcosms that were not dried were incubated at 15 °C without additional methane (at atmospheric levels) during the time of each drying procedure to minimize confounding effects. Afterwards the biomass from dried microcosms was carefully re-suspended in 16 ml MilliQ water to keep salt concentrations similar between treatments and controls and 4 ml of fresh M2 medium were added to both treatments and the controls to minimize nutrient limitation during the experiment. Subsequently, microcosms were incubated as described above until the next perturbation.

Before each dry/wet cycle perturbation 4 ml fresh liquid was taken from all microcosms and spun down in the centrifuge at 20817 ×  g . Cell pellets were stored at −80 °C for further analyses.

DNA Extraction

Cell pellets taken from all microcosms after 59 days of incubation were used to extract total nucleic acids following the protocol described by 36 with the following exceptions: We used a modified extraction buffer (112.87 mM Na 2 HPO 4 /7.12 mM NaH 2 PO 4 , pH 7.5; 5% CTAB, 2% SDS, 2% N-Lauroylsarcosine, and 1 M NaCl), frozen cells pellets were added to lysing matrix E tube (MP Biomedicals, Duiven, the Netherlands) and homogenized using the FastPrep®-24 Classic Instrument (MP Biomedicals) for 45 sec at 6.5 m/s, and nucleic acids were precipitated for 90 min at 4 °C by using 2 volumes of 30% PEG 6000 in 1.6 M NaCl. DNA quality and quantity were determined using a Nano-Drop Spectrophotometer (Thermo Scientific, Madison, WI, USA).

Methane consumption

Methane consumption was measured in each microcosm at the following times: before the first dry/wet cycle perturbation, 1, 3, 6, 17, 36 days after the first dry/wet cycle perturbation, 1 and 5 days after the second dry/wet cycle perturbation, and 1, 5, 13, 23 days after the third dry/wet cycle perturbation. Each time microcosms were opened and aerated before microcosms were re-capped with a butyl rubber stopper (Sigma-Aldrich) and 1% of pure methane was added to the headspace. Microcosms were incubated on a rotary shaker (120 rpm) in the dark at room temperature. Methane consumption was followed by GC-FID analysis (Ultra GC gas chromatograph, Interscience, The Netherlands; Rt-Q-Bond 30 m, 0.32 mm, ID capillary, Restek, USA) over a period of two days, including 5 measurements. Column, injector, and detector temperature was set to 80, 150 and 250 °C, respectively. Helium was used as the carrier gas and hydrogen as burning gas. Methane consumption rates for each concentration per sample were calculated by linear regression using the R version 3.2.5 37 .

Normalized recovery

We used methane consumption to calculate recovery from the first and third dry/wet cycle perturbation. Therefore, the values obtained from disturbed microcosm were divided by the average values of the control microcosms. Once values recovered to the levels of the control we set these values to one, i.e. full recovery from each perturbation.

Illumina sequencing and data processing

DNA samples from Day 59 of the experiment were sent for sequencing the V4 region (515F-907 R, Supplementary Information Table  S3 ) of the bacterial 16S rRNA gene using paired-end sequencing (2 × 250 bp) on an Illumina Miseq instruments. PCR and sample preparation has been described in detail in Ren and colleagues 38 .

Sequencing data was processed using the quantitative insights into microbial ecology (QIIME) pipeline 39 in the standard configuration. In brief, low quality paired end sequence reads were removed (sequence lengths <150 bp and average quality scores <25) and sequences were demultiplexed to assign reads to different samples, resulting in sequences with 395 +/− 5 nucleotides. The data has been archived with the NCBI BioProject (PRJNA421932). The UCLUST method was used for OTU clustering 40 .

Clustering was performed at 97% and chimeras were identified using the ChimeraSlayer reference database 41 . A representative sequence from each OTU was aligned with PyNAST 42 . Taxonomy was assigned using the RDP Classifier from the Ribosomal Database Project downloaded on June 22, 2015 43 .

We performed quantitative PCR (qPCR) to determine abundances of total bacteria and methanotrophs for the water samples before the first dry/wet cycle perturbation and after three, seventeen days after the first dry/wet cycle perturbation, and thirteen days after third dry/wet cycle perturbation. The EUBAC assay was used to quantify the total 16S rDNA gene copies 44 and the pmoA -specific qPCR assays MTOT (total methanotrophs) were used to enumerate methanotrophs 45 . The qPCR assays were performed with primers, primer concentration, and PCR profiles as described by Fierer and colleagues 44 and Pan and colleagues 46 , respectively. All qPCR assays were performed in duplicates. Specificity of the amplicon was verified by melting curve analysis. All analyses were performed with a Rotor-Gene Q real-time PCR cycler (Qiagen, Venlo, Netherlands). To quantify total copy number of each individual assay the Rotor-Gene Q Series Software (Qiagen) was used. pmoA copy numbers were divided by two, which is the average number of this gene in methanotrophic genomes.

Statistical analysis

Statistical and graphical analyses were performed using R version 3.2.5 and 3.3.2 37 . The OTU table from the Illumina sequencing was first rarefied to 2140 sequences per sample using the rrarefy function in the vegan package implemented in R. To test for differences in the community structure we used Analysis of similarities (ANOSIM) based on Bray–Curtis dissimilarities in the vegan package. Nonmetric dimensional scaling (NMDS) was performed using the metaMDS function in the vegan package. The dissimilarity matrix (Bray–Curtis) was calculated with the vegdist function in the vegan package 47 . Heatmaps and graphs were prepared using the gplots package 48 . Diversity parameters, richness, evenness, and Shannon diversity were calculated with function diversity in the vegan package 47 . To evaluate qPCR results we first performed a F-Test, followed by the appropriate T-Test (equal or unequal variance, two-sided).

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

This study was part of the European Science Foundation EUROCORES Programme EuroEEFG and was financially supported by grants from the Netherlands Organization for Scientific Research (NWO) (Grant number 855.01.150, 823.001.008). Many thanks to Dr. Sang Yoon Kim for his help measuring methane oxidation rates. This publication is publication nr. 6532 of the Netherlands Institute of Ecology.

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Sascha M. B. Krause

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands

Sascha M. B. Krause, Marion Meima-Franke, Annelies J. Veraart, Adrian Ho & Paul L. E. Bodelier

Department of Aquatic Ecology and Environmental Biology, Institute for Water and Wetland Research, Radboud University, Nijmegen, The Netherlands

Annelies J. Veraart

Institute of Agricultural Sciences and Environments, Jiangsu Academy of Agricultural Sciences, Nanjing, China

State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China

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S.M.B.K. and P.L.E.B. designed research; S.M.B.K., M.M.-F. and G.R. performed research; S.M.B.K., P.L.E.B., and A.J.V. analyzed data; and S.M.B.K., P.L.E.B., A.J.V., and A.H. wrote the paper.

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Krause, S.M.B., Meima-Franke, M., Veraart, A.J. et al. Environmental legacy contributes to the resilience of methane consumption in a laboratory microcosm system. Sci Rep 8 , 8862 (2018). https://doi.org/10.1038/s41598-018-27168-9

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DOI : https://doi.org/10.1038/s41598-018-27168-9

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Scientists reveal the first unconventional superconductor that can be found in mineral form in nature

by Ames National Laboratory

Scientists from Ames National Laboratory have identified the first unconventional superconductor with a chemical composition also found in nature. Miassite is one of only four minerals found in nature that act as a superconductor when grown in the lab. The team's investigation of miassite revealed that it is an unconventional superconductor with properties similar to high-temperature superconductors.

Their findings , published in Communications Materials , further scientists' understanding of this type of superconductivity, which could lead to more sustainable and economical superconductor-based technology in the future.

Superconductivity is when a material can conduct electricity without energy loss. Superconductors have applications including medical MRI machines, power cables, and quantum computers. Conventional superconductors are well understood but have low critical temperatures. The critical temperature is the highest temperature at which a material acts as a superconductor.

In the 1980s, scientists discovered unconventional superconductors, many of which have much higher critical temperatures. According to Ruslan Prozorov, a scientist at Ames Lab, all these materials are grown in the lab. This fact has led to the general belief that unconventional superconductivity is not a natural phenomenon.

Prozorov explained that it is difficult to find superconductors in nature because most superconducting elements and compounds are metals and tend to react with other elements, like oxygen. He said that miassite (Rh 17 S 15 ) is an interesting mineral for several reasons, one of which is its complex chemical formula. "Intuitively, you think that this is something which is produced deliberately during a focused search, and it cannot possibly exist in nature," said Prozorov, "But it turns out it does."

Paul Canfield, Distinguished Professor of Physics and Astronomy at Iowa State University and a scientist at Ames Lab, has expertise in design, discovery, growth, and characterization of novel crystalline materials. He synthesized high quality miassite crystals for this project. "Although miassite is a mineral that was discovered near the Miass River in Chelyabinsk Oblast, Russia," said Canfield, "it is a rare one that generally does not grow as well-formed crystals."

Growing the miassite crystals was part of a larger effort to discover compounds that combine very high melting elements (like Rh) and volatile elements (like S). "Contrary to the nature of the pure elements, we have been mastering the use of mixtures of these elements that allow for low temperature growth of crystals with minimal vapor pressure," said Canfield.

"It's like finding a hidden fishing hole that is full of big fat fish. In the Rh-S system we discovered three new superconductors. And, through Ruslan's detailed measurements, we discovered that the miassite is an unconventional superconductor."

Prozorov's group specializes in advanced techniques to study superconductors at low temperatures. He said the material needed to be as cold as 50 millikelvins, which is about -460°F.

Prozorov's team used three different tests to determine the nature of miassite's superconductivity. The main test is called the "London penetration depth." It determines how far a weak magnetic field can penetrate the superconductor bulk from the surface. In a conventional superconductor, this length is basically constant at low temperature. However, in unconventional superconductors, it varies linearly with the temperature. This test showed that miassite behaves as an unconventional superconductor.

Another test the team performed was introducing defects into the material. Prozorov said that this test is a signature technique his team has employed over the past decade. It involves bombarding the material with high-energy electrons. This process knocks-out ions from their positions, thus creating defects in the crystal structure. This disorder can cause changes in the material's critical temperature.

Conventional superconductors are not sensitive to non-magnetic disorder, so this test would show no or very little change in the critical temperature. Unconventional superconductors have a high sensitivity to disorder, and introducing defects changes or suppresses the critical temperature. It also affects the critical magnetic field of the material. In miassite, the team found that both the critical temperature and the critical magnetic field behaved as predicted in unconventional superconductors.

Investigating unconventional superconductors improves scientists understanding of how they work. Prozorov explained that this is important because "uncovering the mechanisms behind unconventional superconductivity is key to economically sound applications of superconductors."

Journal information: Communications Materials

Provided by Ames National Laboratory

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