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Global warming modulates soil respiration (RS) via microbial decomposition, which is seasonally dependent. Yet, the magnitude and direction of this modulation remain unclear, partly owing to the lack of knowledge on how microorganisms respond to seasonal changes. Here, we investigated the temporal dynamics of soil microbial communities over 12 consecutive months under experimental warming in a tallgrass prairie ecosystem. The interplay between warming and time altered (P

Increasing soil organic carbon (SOC) in croplands by switching from conventional to conservation management may be hampered by stimulated microbial decomposition under warming. Here, we test the interactive effects of agricultural management and warming on SOC persistence and underlying microbial mechanisms in a decade-long controlled experiment on a wheat-maize cropping system. Warming increased SOC content and accelerated fungal community temporal turnover under conservation agriculture (no tillage, chopped crop residue), but not under conventional agriculture (annual tillage, crop residue removed). Microbial carbon use efficiency (CUE) and growth increased linearly over time, with stronger positive warming effects after 5 years under conservation agriculture. According to structural equation models, these increases arose from greater carbon inputs from the crops, which indirectly controlled microbial CUE via changes in fungal communities. As a result, fungal necromass increased from 28 to 53%, emerging as the strongest predictor of SOC content. Collectively, our results demonstrate how management and climatic factors can interact to alter microbial community composition, physiology and functions and, in turn, SOC formation and accrual in croplands.

Unravelling biosphere feedback mechanisms is crucial for predicting the impacts of global warming. Soil priming, an effect of fresh plant-derived carbon (C) on native soil organic carbon (SOC) decomposition, is a key feedback mechanism that could release large amounts of soil C into the atmosphere. However, the impacts of climate warming on soil priming remain elusive. Here, we show that experimental warming accelerates soil priming by 12.7% in a temperate grassland. Warming alters bacterial communities, with 38% of unique active phylotypes detected under warming. The functional genes essential for soil C decomposition are also stimulated, which could be linked to priming effects. We incorporate lab-derived information into an ecosystem model showing that model parameter uncertainty can be reduced by 32-37%. Model simulations from 2010 to 2016 indicate an increase in soil C decomposition under warming, with a 9.1% rise in priming-induced CO2 emissions. If our findings can be generalized to other ecosystems over an extended period of time, soil priming could play an important role in terrestrial C cycle feedbacks and climate change.

Cobalamin (B12), an essential nutrient and growth cofactor for many living organisms on Earth, can be fully synthesized only by selected prokaryotes in nature. Therefore, microbial communities related to B12 biosynthesis could serve as an example subsystem to disentangle the underlying ecological mechanisms balancing the function and taxonomic make-up of complex functional assemblages. By anchoring microbial traits potentially involved in B12 biosynthesis, we depict the biogeographic patterns of B12 biosynthesis genes and the taxa harboring them in the global ocean, despite the limitations of detecting de novo B12 synthesizers via metagenomes alone. Both the taxonomic and functional composition of B12 biosynthesis genes were strongly shaped by depth, differentiating the epipelagic zones from the mesopelagic layers. Functional genes related to B12 biosynthesis were relatively stably distributed across different oceans, but the taxa harboring them varied considerably, showing clear functional redundancy among microbial systems. Microbial taxa carrying B12 biosynthesis genes in the surface water were influenced by environmental factors such as temperature, oxygen, and nitrate. However, the composition of functional genes was only weakly associated with these environmental factors. Null model analyses demonstrated that determinism governed the variations in B12 biosynthesis genes, whereas a higher degree of stochasticity was associated with taxonomic variations. Significant associations were observed between the chlorophyll a concentration and B12 biosynthesis, confirming its importance in primary production in the global ocean. The results of this study reveal an essential ecological mechanism governing the assembly of microbes in nature: the environment selects for function rather than taxonomy; functional redundancy underlies stochastic community assembly.

Disentangling the assembly mechanisms controlling community composition, structure, distribution, functions, and dynamics is a central issue in ecology. Although various approaches have been proposed to examine community assembly mechanisms, quantitative characterization is challenging, particularly in microbial ecology. Here, we present a novel approach for quantitatively delineating community assembly mechanisms by combining the consumer-resource model with a neutral model in stochastic differential equations. Using time-series data from anaerobic bioreactors that target microbial 16S rRNA genes, we tested the applicability of three ecological models: the consumer-resource model, the neutral model, and the combined model. Our results revealed that model performances varied substantially as a function of population abundance and/or process conditions. The combined model performed best for abundant taxa in the treatment bioreactors where process conditions were manipulated. In contrast, the neutral model showed the best performance for rare taxa. Our analysis further indicated that immigration rates decreased with taxa abundance and competitions between taxa were strongly correlated with phylogeny, but within a certain phylogenetic distance only. The determinism underlying taxa and community dynamics were quantitatively assessed, showing greater determinism in the treatment bioreactors that aligned with the subsequent abnormal system functioning. Given its mechanistic basis, the framework developed here is expected to be potentially applicable beyond microbial ecology.

IntroductionPetroleum pollution resulting from spills and leakages in oil refinery areas has been a significant environmental concern for decades. Despite this, the effects of petroleum pollutants on soil microbial communities and their potential for pollutant biodegradation still required further investigation.MethodsIn this study, we collected 75 soil samples from 0 to 5 m depths of 15 soil profiles in an abandoned refinery to analyze the effect of petroleum pollution on soil microbial diversity, community structure, and network co-occurrence patterns.ResultsOur results suggested soil microbial a-diversity decreased under high C10-C40 levels, coupled with significant changes in the community structure of soil profiles. However, soil microbial network complexity increased with petroleum pollution levels, suggesting more complex microbial potential interactions. A module specific for methane and methyl oxidation was also found under high C10-C40 levels of the soil profile, indicating stronger methanotrophic and methylotrophic metabolic activities at the heavily polluted soil profile.DiscussionThe increased network complexity observed may be due to more metabolic pathways and processes, as well as increased microbial interactions during these processes. These findings highlight the importance of considering both microbial diversity and network complexity in assessing the effects of petroleum pollution on soil ecosystems.

Soil microbial communitys responses to climate warming alter the global carbon cycle. In temperate ecosystems, soil microbial communities function along seasonal cycles. However, little is known about how the responses of soil microbial communities to warming vary when the season changes. In this study, we investigated the seasonal dynamics of soil bacterial community under experimental warming in a temperate tall-grass prairie ecosystem. Our results showed that warming significantly (p = 0.001) shifted community structure, such that the differences of microbial communities between warming and control plots increased nonlinearly (R 2 = 0.578, p = 0.021) from spring to winter. Also, warming significantly (p

Anthropogenic climate change threatens ecosystem functioning. Soil biodiversity is essential for maintaining the health of terrestrial systems, but how climate change affects the richness and abundance of soil microbial communities remains unresolved. We examined the effects of warming, altered precipitation and annual biomass removal on grassland soil bacterial, fungal and protistan communities over 7 years to determine how these representative climate changes impact microbial biodiversity and ecosystem functioning. We show that experimental warming and the concomitant reductions in soil moisture play a predominant role in shaping microbial biodiversity by decreasing the richness of bacteria (9.6%), fungi (14.5%) and protists (7.5%). Our results also show positive associations between microbial biodiversity and ecosystem functional processes, such as gross primary productivity and microbial biomass. We conclude that the detrimental effects of biodiversity loss might be more severe in a warmer world.

Soil carbon (C) and nitrogen (N) cycles and their complex responses to environmental changes have received increasing attention. However, large uncertainties in model predictions remain, partially due to the lack of explicit representation and parameterization of microbial processes. One great challenge is to effectively integrate rich microbial functional traits into ecosystem modeling for better predictions. Here, using soil enzymes as indicators of soil function, we developed a competitive dynamic enzyme allocation scheme and detailed enzyme-mediated soil inorganic N processes in the Microbial-ENzyme Decomposition (MEND) model. We conducted a rigorous calibration and validation of MEND with diverse soil C-N fluxes, microbial C:N ratios, and functional gene abundances from a 12-year CO2  × N grassland experiment (BioCON) in Minnesota, USA. In addition to accurately simulating soil CO2 fluxes and multiple N variables, the model correctly predicted microbial C:N ratios and their negative response to enriched N supply. Model validation further showed that, compared to the changes in simulated enzyme concentrations and decomposition rates, the changes in simulated activities of eight C-N-associated enzymes were better explained by the measured gene abundances in responses to elevated atmospheric CO2 concentration. Our results demonstrated that using enzymes as indicators of soil function and validating model predictions with functional gene abundances in ecosystem modeling can provide a basis for testing hypotheses about microbially mediated biogeochemical processes in response to environmental changes. Further development and applications of the modeling framework presented here will enable microbial ecologists to address ecosystem-level questions beyond empirical observations, toward more predictive understanding, an ultimate goal of microbial ecology.

The recent application of macroecological tools and concepts has made it possible to identify consistent patterns in the distribution of microbial biodiversity, which greatly improved our understanding of the microbial world at large scales. However, the distribution of microbial functions remains largely uncharted from the macroecological point of view. Here, we used macroecological models to examine how the genes encoding the functional capabilities of microorganisms are distributed within and across soil systems. Models built using functional gene array data from 818 soil microbial communities showed that the occupancy-frequency distributions of genes were bimodal in every studied site, and that their rank-abundance distributions were best described by a lognormal model. In addition, the relationships between gene occupancy and abundance were positive in all sites. This allowed us to identify genes with high abundance and ubiquitous distribution (core) and genes with low abundance and limited spatial distribution (satellites), and to show that they encode different sets of microbial traits. Common genes encode microbial traits related to the main biogeochemical cycles (C, N, P and S) while rare genes encode traits related to adaptation to environmental stresses, such as nutrient limitation, resistance to heavy metals and degradation of xenobiotics. Overall, this study characterized for the first time the distribution of microbial functional genes within soil systems, and highlight the interest of macroecological models for understanding the functional organization of microbial systems across spatial scales.

Nutrient scarcity is pervasive for natural microbial communities, affecting species reproduction and co-existence. However, it remains unclear whether there are general rules of how microbial species abundances are shaped by biotic and abiotic factors. Here we show that the ribosomal RNA gene operon (rrn) copy number, a genomic trait related to bacterial growth rate and nutrient demand, decreases from the abundant to the rare biosphere in the nutrient-rich coastal sediment but exhibits the opposite pattern in the nutrient-scarce pelagic zone of the global ocean. Both patterns are underlain by positive correlations between community-level rrn copy number and nutrients. Furthermore, inter-species co-exclusion inferred by negative network associations is observed more in coastal sediment than in ocean water samples. Nutrient manipulation experiments yield effects of nutrient availability on rrn copy numbers and network associations that are consistent with our field observations. Based on these results, we propose a "hunger games" hypothesis to define microbial species abundance rules using the rrn copy number, ecological interaction, and nutrient availability.

BackgroundAnthropogenic activities have increased the inputs of atmospheric reactive nitrogen (N) into terrestrial ecosystems, affecting soil carbon stability and microbial communities. Previous studies have primarily examined the effects of nitrogen deposition on microbial taxonomy, enzymatic activities, and functional processes. Here, we examined various functional traits of soil microbial communities and how these traits are interrelated in a Mediterranean-type grassland administrated with 14 years of 7 g m-2 year-1 of N amendment, based on estimated atmospheric N deposition in areas within California, USA, by the end of the twenty-first century.ResultsSoil microbial communities were significantly altered by N deposition. Consistent with higher aboveground plant biomass and litter, fast-growing bacteria, assessed by abundance-weighted average rRNA operon copy number, were favored in N deposited soils. The relative abundances of genes associated with labile carbon (C) degradation (e.g., amyA and cda) were also increased. In contrast, the relative abundances of functional genes associated with the degradation of more recalcitrant C (e.g., mannanase and chitinase) were either unchanged or decreased. Compared with the ambient control, N deposition significantly reduced network complexity, such as average degree and connectedness. The network for N deposited samples contained only genes associated with C degradation, suggesting that C degradation genes became more intensely connected under N deposition.ConclusionsWe propose a conceptual model to summarize the mechanisms of how changes in above- and belowground ecosystems by long-term N deposition collectively lead to more soil C accumulation. Video Abstract.

Switchgrass is a deep-rooted perennial native to the US prairies and an attractive feedstock for bioenergy production; when cultivated on marginal soils it can provide a potential mechanism to sequester and accumulate soil carbon (C). However, the impacts of switchgrass establishment on soil biotic/abiotic properties are poorly understood. Additionally, few studies have reported the effects of switchgrass cultivation on marginal lands that have low soil nutrient quality (N/P) or in areas that have experienced high rates of soil erosion. Here, we report a comparative analyses of soil greenhouse gases (GHG), soil chemistry, and microbial communities in two contrasting soil types (with or without switchgrass) over 17 months (1428 soil samples). These soils are highly eroded, 'Dust Bowl' remnant field sites in southern Oklahoma, USA. Our results revealed that soil C significantly increased at the sandy-loam (SL) site, but not at the clay-loam (CL) site. Significantly higher CO2 flux was observed from the CL switchgrass site, along with reduced microbial diversity (both alpha and beta). Strikingly, methane (CH4) consumption was significantly reduced by an estimated 39 and 47% at the SL and CL switchgrass sites, respectively. Together, our results suggest that soil C stocks and GHG fluxes are distinctly different at highly degraded sites when switchgrass has been cultivated, implying that carbon balance considerations should be accounted for to fully evaluate the sustainability of deep-rooted perennial grass cultivation in marginal lands.

Switchgrass is a deep-rooted perennial native to the US prairies and an attractive feedstock for bioenergy production; when cultivated on marginal soils it can provide a potential mechanism to sequester and accumulate soil carbon (C). However, the impacts of switchgrass establishment on soil biotic/abiotic properties are poorly understood. Additionally, few studies have reported the effects of switchgrass cultivation on marginal lands that have low soil nutrient quality (N/P) or in areas that have experienced high rates of soil erosion. Here, we report a comparative analyses of soil greenhouse gases (GHG), soil chemistry, and microbial communities in two contrasting soil types (with or without switchgrass) over 17 months (1428 soil samples). These soils are highly eroded, 'Dust Bowl' remnant field sites in southern Oklahoma, USA. Our results revealed that soil C significantly increased at the sandy-loam (SL) site, but not at the clay-loam (CL) site. Significantly higher CO2 flux was observed from the CL switchgrass site, along with reduced microbial diversity (both alpha and beta). Strikingly, methane (CH4) consumption was significantly reduced by an estimated 39 and 47% at the SL and CL switchgrass sites, respectively. Together, our results suggest that soil C stocks and GHG fluxes are distinctly different at highly degraded sites when switchgrass has been cultivated, implying that carbon balance considerations should be accounted for to fully evaluate the sustainability of deep-rooted perennial grass cultivation in marginal lands.

As the second-largest terrestrial carbon (C) flux, soil respiration (RS) has been stimulated by climate warming. However, the magnitude and dynamics of such stimulations of soil respiration are highly uncertain at the global scale, undermining our confidence in future climate projections. Here, we present an analysis of global RS observations from 1987-2016. RS increased (P

Whether and how CO2 and nitrogen (N) availability interact to influence carbon (C) cycling processes such as soil respiration remains a question of considerable uncertainty in projecting future C-climate feedbacks, which are strongly influenced by multiple global change drivers, including elevated atmospheric CO2 concentrations (eCO2) and increased N deposition. However, because decades of research on the responses of ecosystems to eCO2 and N enrichment have been done largely independently, their interactive effects on soil respiratory CO2 efflux remain unresolved. Here, we show that in a multifactor free-air CO2 enrichment experiment, BioCON (Biodiversity, CO2, and N deposition) in Minnesota, the positive response of soil respiration to eCO2 gradually strengthened at ambient (low) N supply but not enriched (high) N supply for the 12-y experimental period from 1998 to 2009. In contrast to earlier years, eCO2 stimulated soil respiration twice as much at low than at high N supply from 2006 to 2009. In parallel, microbial C degradation genes were significantly boosted by eCO2 at low but not high N supply. Incorporating those functional genes into a coupled C-N ecosystem model reduced model parameter uncertainty and improved the projections of the effects of different CO2 and N levels on soil respiration. If our observed results generalize to other ecosystems, they imply widely positive effects of eCO2 on soil respiration even in infertile systems.

BackgroundIt is well-known that global warming has effects on high-latitude tundra underlain with permafrost. This leads to a severe concern that decomposition of soil organic carbon (SOC) previously stored in this region, which accounts for about 50% of the world's SOC storage, will cause positive feedback that accelerates climate warming. We have previously shown that short-term warming (1.5 years) stimulates rapid, microbe-mediated decomposition of tundra soil carbon without affecting the composition of the soil microbial community (based on the depth of 42684 sequence reads of 16S rRNA gene amplicons per 3 g of soil sample).ResultsWe show that longer-term (5 years) experimental winter warming at the same site altered microbial communities (p < 0.040). Thaw depth correlated the strongest with community assembly and interaction networks, implying that warming-accelerated tundra thaw fundamentally restructured the microbial communities. Both carbon decomposition and methanogenesis genes increased in relative abundance under warming, and their functional structures strongly correlated (R2 > 0.725, p < 0.001) with ecosystem respiration or CH4 flux.ConclusionsOur results demonstrate that microbial responses associated with carbon cycling could lead to positive feedbacks that accelerate SOC decomposition in tundra regions, which is alarming because SOC loss is unlikely to subside owing to changes in microbial community composition. Video Abstract.

BackgroundIn a warmer world, microbial decomposition of previously frozen organic carbon (C) is one of the most likely positive climate feedbacks of permafrost regions to the atmosphere. However, mechanistic understanding of microbial mediation on chemically recalcitrant C instability is limited; thus, it is crucial to identify and evaluate active decomposers of chemically recalcitrant C, which is essential for predicting C-cycle feedbacks and their relative strength of influence on climate change. Using stable isotope probing of the active layer of Arctic tundra soils after depleting soil labile C through a 975-day laboratory incubation, the identity of microbial decomposers of lignin and, their responses to warming were revealed.ResultsThe β-Proteobacteria genus Burkholderia accounted for 95.1% of total abundance of potential lignin decomposers. Consistently, Burkholderia isolated from our tundra soils could grow with lignin as the sole C source. A 2.2 °C increase of warming considerably increased total abundance and functional capacities of all potential lignin decomposers. In addition to Burkholderia, α-Proteobacteria capable of lignin decomposition (e.g. Bradyrhizobium and Methylobacterium genera) were stimulated by warming by 82-fold. Those community changes collectively doubled the priming effect, i.e., decomposition of existing C after fresh C input to soil. Consequently, warming aggravates soil C instability, as verified by microbially enabled climate-C modeling.ConclusionsOur findings are alarming, which demonstrate that accelerated C decomposition under warming conditions will make tundra soils a larger biospheric C source than anticipated. Video Abstract.

BackgroundThe newly defined superphylum Patescibacteria such as Parcubacteria (OD1) and Microgenomates (OP11) has been found to be prevalent in groundwater, sediment, lake, and other aquifer environments. Recently increasing attention has been paid to this diverse superphylum including > 20 candidate phyla (a large part of the candidate phylum radiation, CPR) because it refreshed our view of the tree of life. However, adaptive traits contributing to its prevalence are still not well known.ResultsHere, we investigated the genomic features and metabolic pathways of Patescibacteria in groundwater through genome-resolved metagenomics analysis of > 600 Gbp sequence data. We observed that, while the members of Patescibacteria have reduced genomes (~ 1 Mbp) exclusively, functions essential to growth and reproduction such as genetic information processing were retained. Surprisingly, they have sharply reduced redundant and nonessential functions, including specific metabolic activities and stress response systems. The Patescibacteria have ultra-small cells and simplified membrane structures, including flagellar assembly, transporters, and two-component systems. Despite the lack of CRISPR viral defense, the bacteria may evade predation through deletion of common membrane phage receptors and other alternative strategies, which may explain the low representation of prophage proteins in their genomes and lack of CRISPR. By establishing the linkages between bacterial features and the groundwater environmental conditions, our results provide important insights into the functions and evolution of this CPR group.ConclusionsWe found that Patescibacteria has streamlined many functions while acquiring advantages such as avoiding phage invasion, to adapt to the groundwater environment. The unique features of small genome size, ultra-small cell size, and lacking CRISPR of this large lineage are bringing new understandings on life of Bacteria. Our results provide important insights into the mechanisms for adaptation of the superphylum in the groundwater environments, and demonstrate a case where less is more, and small is mighty.

Soil microbial respiration is an important source of uncertainty in projecting future climate and carbon (C) cycle feedbacks. However, its feedbacks to climate warming and underlying microbial mechanisms are still poorly understood. Here we show that the temperature sensitivity of soil microbial respiration (Q10) in a temperate grassland ecosystem persistently decreases by 12.0 ± 3.7% across 7 years of warming. Also, the shifts of microbial communities play critical roles in regulating thermal adaptation of soil respiration. Incorporating microbial functional gene abundance data into a microbially-enabled ecosystem model significantly improves the modeling performance of soil microbial respiration by 5-19%, and reduces model parametric uncertainty by 55-71%. In addition, modeling analyses show that the microbial thermal adaptation can lead to considerably less heterotrophic respiration (11.6 ± 7.5%), and hence less soil C loss. If such microbially mediated dampening effects occur generally across different spatial and temporal scales, the potential positive feedback of soil microbial respiration in response to climate warming may be less than previously predicted.

Unraveling the drivers controlling community assembly is a central issue in ecology. Although it is generally accepted that selection, dispersal, diversification and drift are major community assembly processes, defining their relative importance is very challenging. Here, we present a framework to quantitatively infer community assembly mechanisms by phylogenetic bin-based null model analysis (iCAMP). iCAMP shows high accuracy (0.93-0.99), precision (0.80-0.94), sensitivity (0.82-0.94), and specificity (0.95-0.98) on simulated communities, which are 10-160% higher than those from the entire community-based approach. Application of iCAMP to grassland microbial communities in response to experimental warming reveals dominant roles of homogeneous selection (38%) and 'drift' (59%). Interestingly, warming decreases 'drift' over time, and enhances homogeneous selection which is primarily imposed on Bacillales. In addition, homogeneous selection has higher correlations with drought and plant productivity under warming than control. iCAMP provides an effective and robust tool to quantify microbial assembly processes, and should also be useful for plant and animal ecology.

BACKGROUND: In a warmer world, microbial decomposition of previously frozen organic carbon (C) is one of the most likely positive climate feedbacks of permafrost regions to the atmosphere. However, mechanistic understanding of microbial mediation on chemically recalcitrant C instability is limited; thus, it is crucial to identify and evaluate active decomposers of chemically recalcitrant C, which is essential for predicting C-cycle feedbacks and their relative strength of influence on climate change. Using stable isotope probing of the active layer of Arctic tundra soils after depleting soil labile C through a 975-day laboratory incubation, the identity of microbial decomposers of lignin and, their responses to warming were revealed. RESULTS: The β-Proteobacteria genus Burkholderia accounted for 95.1% of total abundance of potential lignin decomposers. Consistently, Burkholderia isolated from our tundra soils could grow with lignin as the sole C source. A 2.2 °C increase of warming considerably increased total abundance and functional capacities of all potential lignin decomposers. In addition to Burkholderia, α-Proteobacteria capable of lignin decomposition (e.g. Bradyrhizobium and Methylobacterium genera) were stimulated by warming by 82-fold. Those community changes collectively doubled the priming effect, i.e., decomposition of existing C after fresh C input to soil. Consequently, warming aggravates soil C instability, as verified by microbially enabled climate-C modeling. CONCLUSIONS: Our findings are alarming, which demonstrate that accelerated C decomposition under warming conditions will make tundra soils a larger biospheric C source than anticipated. Video Abstract.

BackgroundIn a warmer world, microbial decomposition of previously frozen organic carbon (C) is one of the most likely positive climate feedbacks of permafrost regions to the atmosphere. However, mechanistic understanding of microbial mediation on chemically recalcitrant C instability is limited; thus, it is crucial to identify and evaluate active decomposers of chemically recalcitrant C, which is essential for predicting C-cycle feedbacks and their relative strength of influence on climate change. Using stable isotope probing of the active layer of Arctic tundra soils after depleting soil labile C through a 975-day laboratory incubation, the identity of microbial decomposers of lignin and, their responses to warming were revealed.ResultsThe β-Proteobacteria genus Burkholderia accounted for 95.1% of total abundance of potential lignin decomposers. Consistently, Burkholderia isolated from our tundra soils could grow with lignin as the sole C source. A 2.2 °C increase of warming considerably increased total abundance and functional capacities of all potential lignin decomposers. In addition to Burkholderia, α-Proteobacteria capable of lignin decomposition (e.g. Bradyrhizobium and Methylobacterium genera) were stimulated by warming by 82-fold. Those community changes collectively doubled the priming effect, i.e., decomposition of existing C after fresh C input to soil. Consequently, warming aggravates soil C instability, as verified by microbially enabled climate-C modeling.ConclusionsOur findings are alarming, which demonstrate that accelerated C decomposition under warming conditions will make tundra soils a larger biospheric C source than anticipated. Video Abstract.

BackgroundThe newly defined superphylum Patescibacteria such as Parcubacteria (OD1) and Microgenomates (OP11) has been found to be prevalent in groundwater, sediment, lake, and other aquifer environments. Recently increasing attention has been paid to this diverse superphylum including > 20 candidate phyla (a large part of the candidate phylum radiation, CPR) because it refreshed our view of the tree of life. However, adaptive traits contributing to its prevalence are still not well known.ResultsHere, we investigated the genomic features and metabolic pathways of Patescibacteria in groundwater through genome-resolved metagenomics analysis of > 600 Gbp sequence data. We observed that, while the members of Patescibacteria have reduced genomes (~ 1 Mbp) exclusively, functions essential to growth and reproduction such as genetic information processing were retained. Surprisingly, they have sharply reduced redundant and nonessential functions, including specific metabolic activities and stress response systems. The Patescibacteria have ultra-small cells and simplified membrane structures, including flagellar assembly, transporters, and two-component systems. Despite the lack of CRISPR viral defense, the bacteria may evade predation through deletion of common membrane phage receptors and other alternative strategies, which may explain the low representation of prophage proteins in their genomes and lack of CRISPR. By establishing the linkages between bacterial features and the groundwater environmental conditions, our results provide important insights into the functions and evolution of this CPR group.ConclusionsWe found that Patescibacteria has streamlined many functions while acquiring advantages such as avoiding phage invasion, to adapt to the groundwater environment. The unique features of small genome size, ultra-small cell size, and lacking CRISPR of this large lineage are bringing new understandings on life of Bacteria. Our results provide important insights into the mechanisms for adaptation of the superphylum in the groundwater environments, and demonstrate a case where less is more, and small is mighty.

Fire is a crucial event regulating the structure and functioning of many ecosystems. Yet few studies have focused on how fire affects taxonomic and functional diversities of soil microbial communities, along with changes in plant communities and soil carbon (C) and nitrogen (N) dynamics. Here, we analyze these effects in a grassland ecosystem 9 months after an experimental fire at the Jasper Ridge Global Change Experiment site in California, USA. Fire altered soil microbial communities considerably, with community assembly process analysis showing that environmental selection pressure was higher in burned sites. However, a small subset of highly connected taxa was able to withstand the disturbance. In addition, fire decreased the relative abundances of most functional genes associated with C degradation and N cycling, implicating a slowdown of microbial processes linked to soil C and N dynamics. In contrast, fire stimulated above- and belowground plant growth, likely enhancing plant-microbe competition for soil inorganic N, which was reduced by a factor of about 2. To synthesize those findings, we performed structural equation modeling, which showed that plants but not microbial communities were responsible for significantly higher soil respiration rates in burned sites. Together, our results demonstrate that fire 'reboots' the grassland ecosystem by differentially regulating plant and soil microbial communities, leading to significant changes in soil C and N dynamics.

Fire is a crucial event regulating the structure and functioning of many ecosystems. Yet few studies have focused on how fire affects taxonomic and functional diversities of soil microbial communities, along with changes in plant communities and soil carbon (C) and nitrogen (N) dynamics. Here, we analyze these effects in a grassland ecosystem 9 months after an experimental fire at the Jasper Ridge Global Change Experiment site in California, USA. Fire altered soil microbial communities considerably, with community assembly process analysis showing that environmental selection pressure was higher in burned sites. However, a small subset of highly connected taxa was able to withstand the disturbance. In addition, fire decreased the relative abundances of most functional genes associated with C degradation and N cycling, implicating a slowdown of microbial processes linked to soil C and N dynamics. In contrast, fire stimulated above- and belowground plant growth, likely enhancing plant-microbe competition for soil inorganic N, which was reduced by a factor of about 2. To synthesize those findings, we performed structural equation modeling, which showed that plants but not microbial communities were responsible for significantly higher soil respiration rates in burned sites. Together, our results demonstrate that fire 'reboots' the grassland ecosystem by differentially regulating plant and soil microbial communities, leading to significant changes in soil C and N dynamics.

BACKGROUND: It is well-known that global warming has effects on high-latitude tundra underlain with permafrost. This leads to a severe concern that decomposition of soil organic carbon (SOC) previously stored in this region, which accounts for about 50% of the worlds SOC storage, will cause positive feedback that accelerates climate warming. We have previously shown that short-term warming (1.5 years) stimulates rapid, microbe-mediated decomposition of tundra soil carbon without affecting the composition of the soil microbial community (based on the depth of 42684 sequence reads of 16S rRNA gene amplicons per 3 g of soil sample). RESULTS: We show that longer-term (5 years) experimental winter warming at the same site altered microbial communities (p < 0.040). Thaw depth correlated the strongest with community assembly and interaction networks, implying that warming-accelerated tundra thaw fundamentally restructured the microbial communities. Both carbon decomposition and methanogenesis genes increased in relative abundance under warming, and their functional structures strongly correlated (R2 > 0.725, p < 0.001) with ecosystem respiration or CH4 flux. CONCLUSIONS: Our results demonstrate that microbial responses associated with carbon cycling could lead to positive feedbacks that accelerate SOC decomposition in tundra regions, which is alarming because SOC loss is unlikely to subside owing to changes in microbial community composition. Video Abstract.

BACKGROUND:It is well-known that global warming has effects on high-latitude tundra underlain with permafrost. This leads to a severe concern that decomposition of soil organic carbon (SOC) previously stored in this region, which accounts for about 50% of the world's SOC storage, will cause positive feedback that accelerates climate warming. We have previously shown that short-term warming (1.5 years) stimulates rapid, microbe-mediated decomposition of tundra soil carbon without affecting the composition of the soil microbial community (based on the depth of 42684 sequence reads of 16S rRNA gene amplicons per 3 g of soil sample). RESULTS:We show that longer-term (5 years) experimental winter warming at the same site altered microbial communities (p < 0.040). Thaw depth correlated the strongest with community assembly and interaction networks, implying that warming-accelerated tundra thaw fundamentally restructured the microbial communities. Both carbon decomposition and methanogenesis genes increased in relative abundance under warming, and their functional structures strongly correlated (R2 > 0.725, p < 0.001) with ecosystem respiration or CH4 flux. CONCLUSIONS:Our results demonstrate that microbial responses associated with carbon cycling could lead to positive feedbacks that accelerate SOC decomposition in tundra regions, which is alarming because SOC loss is unlikely to subside owing to changes in microbial community composition. Video Abstract.

Soil microbial respiration is an important source of uncertainty in projecting future climate and carbon (C) cycle feedbacks. However, its feedbacks to climate warming and underlying microbial mechanisms are still poorly understood. Here we show that the temperature sensitivity of soil microbial respiration (Q10) in a temperate grassland ecosystem persistently decreases by 12.0 ± 3.7% across 7 years of warming. Also, the shifts of microbial communities play critical roles in regulating thermal adaptation of soil respiration. Incorporating microbial functional gene abundance data into a microbially-enabled ecosystem model significantly improves the modeling performance of soil microbial respiration by 5-19%, and reduces model parametric uncertainty by 55-71%. In addition, modeling analyses show that the microbial thermal adaptation can lead to considerably less heterotrophic respiration (11.6 ± 7.5%), and hence less soil C loss. If such microbially mediated dampening effects occur generally across different spatial and temporal scales, the potential positive feedback of soil microbial respiration in response to climate warming may be less than previously predicted.

Unraveling the drivers controlling community assembly is a central issue in ecology. Although it is generally accepted that selection, dispersal, diversification and drift are major community assembly processes, defining their relative importance is very challenging. Here, we present a framework to quantitatively infer community assembly mechanisms by phylogenetic bin-based null model analysis (iCAMP). iCAMP shows high accuracy (0.93-0.99), precision (0.80-0.94), sensitivity (0.82-0.94), and specificity (0.95-0.98) on simulated communities, which are 10-160% higher than those from the entire community-based approach. Application of iCAMP to grassland microbial communities in response to experimental warming reveals dominant roles of homogeneous selection (38%) and 'drift' (59%). Interestingly, warming decreases 'drift' over time, and enhances homogeneous selection which is primarily imposed on Bacillales. In addition, homogeneous selection has higher correlations with drought and plant productivity under warming than control. iCAMP provides an effective and robust tool to quantify microbial assembly processes, and should also be useful for plant and animal ecology.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Functional diversity is increasingly recognized by microbial ecologists as the essential link between biodiversity patterns and ecosystem functioning, determining the trophic relationships and interactions between microorganisms, their participation in biogeochemical cycles, and their responses to environmental changes. Consequently, its definition and quantification have practical and theoretical implications. In this opinion paper, we present a synthesis on the concept of microbial functional diversity from its definition to its application. Initially, we revisit to the original definition of functional diversity, highlighting two fundamental aspects, the ecological unit under study and the functional traits used to characterize it. Then, we discuss how the particularities of the microbial world disallow the direct application of the concepts and tools developed for macroorganisms. Next, we provide a synthesis of the literature on the types of ecological units and functional traits available in microbial functional ecology. We also provide a list of more than 400 traits covering a wide array of environmentally relevant functions. Lastly, we provide examples of the use of functional diversity in microbial systems based on the different units and traits discussed herein. It is our hope that this paper will stimulate discussions and help the growing field of microbial functional ecology to realize a potential that thus far has only been attained in macrobial ecology.

Nitrogen (N) deposition is a component of global change that has considerable impact on belowground carbon (C) dynamics. Plant growth stimulation and alterations of fungal community composition and functions are the main mechanisms driving soil C gains following N deposition in N-limited temperate forests. In N-rich tropical forests, however, N deposition generally has minor effects on plant growth; consequently, C storage in soil may strongly depend on the microbial processes that drive litter and soil organic matter decomposition. Here, we investigated how microbial functions in old-growth tropical forest soil responded to 13 years of N addition at four rates: 0 (Control), 50 (Low-N), 100 (Medium-N), and 150 (High-N) kg N ha-1  year-1 . Soil organic carbon (SOC) content increased under High-N, corresponding to a 33% decrease in CO2 efflux, and reductions in relative abundances of bacteria as well as genes responsible for cellulose and chitin degradation. A 113% increase in N2 O emission was positively correlated with soil acidification and an increase in the relative abundances of denitrification genes (narG and norB). Soil acidification induced by N addition decreased available P concentrations, and was associated with reductions in the relative abundance of phytase. The decreased relative abundance of bacteria and key functional gene groups for C degradation were related to slower SOC decomposition, indicating the key mechanisms driving SOC accumulation in the tropical forest soil subjected to High-N addition. However, changes in microbial functional groups associated with N and P cycling led to coincidentally large increases in N2 O emissions, and exacerbated soil P deficiency. These two factors partially offset the perceived beneficial effects of N addition on SOC storage in tropical forest soils. These findings suggest a potential to incorporate microbial community and functions into Earth system models considering their effects on greenhouse gas emission, biogeochemical processes, and biodiversity of tropical ecosystems.

Nitrogen (N) deposition is a component of global change that has considerable impact on belowground carbon (C) dynamics. Plant growth stimulation and alterations of fungal community composition and functions are the main mechanisms driving soil C gains following N deposition in N-limited temperate forests. In N-rich tropical forests, however, N deposition generally has minor effects on plant growth; consequently, C storage in soil may strongly depend on the microbial processes that drive litter and soil organic matter decomposition. Here, we investigated how microbial functions in old-growth tropical forest soil responded to 13 years of N addition at four rates: 0 (Control), 50 (Low-N), 100 (Medium-N), and 150 (High-N) kg N ha-1  year-1 . Soil organic carbon (SOC) content increased under High-N, corresponding to a 33% decrease in CO2 efflux, and reductions in relative abundances of bacteria as well as genes responsible for cellulose and chitin degradation. A 113% increase in N2 O emission was positively correlated with soil acidification and an increase in the relative abundances of denitrification genes (narG and norB). Soil acidification induced by N addition decreased available P concentrations, and was associated with reductions in the relative abundance of phytase. The decreased relative abundance of bacteria and key functional gene groups for C degradation were related to slower SOC decomposition, indicating the key mechanisms driving SOC accumulation in the tropical forest soil subjected to High-N addition. However, changes in microbial functional groups associated with N and P cycling led to coincidentally large increases in N2 O emissions, and exacerbated soil P deficiency. These two factors partially offset the perceived beneficial effects of N addition on SOC storage in tropical forest soils. These findings suggest a potential to incorporate microbial community and functions into Earth system models considering their effects on greenhouse gas emission, biogeochemical processes, and biodiversity of tropical ecosystems.

Functional diversity is increasingly recognized by microbial ecologists as the essential link between biodiversity patterns and ecosystem functioning, determining the trophic relationships and interactions between microorganisms, their participation in biogeochemical cycles, and their responses to environmental changes. Consequently, its definition and quantification have practical and theoretical implications. In this opinion paper, we present a synthesis on the concept of microbial functional diversity from its definition to its application. Initially, we revisit to the original definition of functional diversity, highlighting two fundamental aspects, the ecological unit under study and the functional traits used to characterize it. Then, we discuss how the particularities of the microbial world disallow the direct application of the concepts and tools developed for macroorganisms. Next, we provide a synthesis of the literature on the types of ecological units and functional traits available in microbial functional ecology. We also provide a list of more than 400 traits covering a wide array of environmentally relevant functions. Lastly, we provide examples of the use of functional diversity in microbial systems based on the different units and traits discussed herein. It is our hope that this paper will stimulate discussions and help the growing field of microbial functional ecology to realize a potential that thus far has only been attained in macrobial ecology.

Aim: The factors driving microbial community β-diversity (variation in composition) at different spatial scales yield fundamental insights into the mechanisms that maintain ecosystem biodiversity, which as yet are uncertain. Here, we explore whether spatial scale-dependent patterns of β-diversity vary between microbial functional groups and bacterial taxa (i.e., diazotrophic and bacterial communities) across local to regional scales (from metres to hundreds of kilometres). Location: Eastern China. Time period: October and November 2015. Major taxa studied: Diazotrophic and bacterial communities. Methods We use two complementary statistical tools to unveil biotic mechanisms (i.e., species association) underlying variation in β-diversity of diazotrophic and bacterial communities. We examined distance–decay slopes of both communities at the local (1–113 m), meso- (3.4–39 km) and regional (103–668 km) scales. We used an environmentally constrained checkerboard score and topological features of association networks as indices of species association. We then calculated contributions of species association, abiotic factors and geographical distance to explain community β-diversity. The scale-dependent distance–decay relationships were also examined in ubiquitous (high occupancy across samples) and endemic communities of diazotrophs and bacteria. Results Diazotrophs displayed steeper distance–decay slopes than bacteria, suggesting that the β-diversity of diazotrophic communities was more variable. The distance–decay slopes were dependent on spatial scales in both communities, owing to different contributions of geographical distance, abiotic factors and species association at three spatial scales. Intriguingly, species association was greater and contributed more to community β-diversity than other forces at the local scale, implying that species association could greatly alter community structures. Main conclusions Drivers of diazotrophic and bacterial community β-diversity depended on spatial scales, resulting in different distance–decay patterns. Moreover, this was the first study to use two methods to demonstrate that species association played important, but as yet unrecognized, roles in driving spatial scale-dependent β-diversity.

Microorganisms in wastewater treatment plants (WWTPs) are essential for water purification to protect public and environmental health. However, the diversity of microorganisms and the factors that control it are poorly understood. Using a systematic global-sampling effort, we analysed the 16S ribosomal RNA gene sequences from ~1,200 activated sludge samples taken from 269 WWTPs in 23 countries on 6 continents. Our analyses revealed that the global activated sludge bacterial communities contain ~1 billion bacterial phylotypes with a Poisson lognormal diversity distribution. Despite this high diversity, activated sludge has a small, global core bacterial community (n = 28 operational taxonomic units) that is strongly linked to activated sludge performance. Meta-analyses with global datasets associate the activated sludge microbiomes most closely to freshwater populations. In contrast to macroorganism diversity, activated sludge bacterial communities show no latitudinal gradient. Furthermore, their spatial turnover is scale-dependent and appears to be largely driven by stochastic processes (dispersal and drift), although deterministic factors (temperature and organic input) are also important. Our findings enhance our mechanistic understanding of the global diversity and biogeography of activated sludge bacterial communities within a theoretical ecology framework and have important implications for microbial ecology and wastewater treatment processes.

Microorganisms in wastewater treatment plants (WWTPs) are essential for water purification to protect public and environmental health. However, the diversity of microorganisms and the factors that control it are poorly understood. Using a systematic global-sampling effort, we analysed the 16S ribosomal RNA gene sequences from ~1,200 activated sludge samples taken from 269 WWTPs in 23 countries on 6 continents. Our analyses revealed that the global activated sludge bacterial communities contain ~1 billion bacterial phylotypes with a Poisson lognormal diversity distribution. Despite this high diversity, activated sludge has a small, global core bacterial community (n = 28 operational taxonomic units) that is strongly linked to activated sludge performance. Meta-analyses with global datasets associate the activated sludge microbiomes most closely to freshwater populations. In contrast to macroorganism diversity, activated sludge bacterial communities show no latitudinal gradient. Furthermore, their spatial turnover is scale-dependent and appears to be largely driven by stochastic processes (dispersal and drift), although deterministic factors (temperature and organic input) are also important. Our findings enhance our mechanistic understanding of the global diversity and biogeography of activated sludge bacterial communities within a theoretical ecology framework and have important implications for microbial ecology and wastewater treatment processes.

Mild disturbances are prevalent in the environment, which may not be easily notable but could have considerable ecological consequences over prolonged periods. To evaluate this, a field study was designed to examine the effects of very light-intensity lamb grazing on grassland soil microbiomes with different soil backgrounds. No significant change (P > 0.05) was observed in any vegetation and soil variables. Nonetheless, hundreds of microbial functional gene families, but not bacterial taxonomy, were significantly (P

Mild disturbances are prevalent in the environment, which may not be easily notable but could have considerable ecological consequences over prolonged periods. To evaluate this, a field study was designed to examine the effects of very light-intensity lamb grazing on grassland soil microbiomes with different soil backgrounds. No significant change (P > 0.05) was observed in any vegetation and soil variables. Nonetheless, hundreds of microbial functional gene families, but not bacterial taxonomy, were significantly (P

Anaerobic digestion is one of the most successful waste management strategies worldwide, wherein microorganisms play an essential role in reducing organic pollutants and producing renewable energy. However, variations of microbial community in full-scale anaerobic digesters, particularly functional groups relevant to biogas production, remain elusive. Here, we examined microbial community in a year-long monthly time series of 3 full-scale anaerobic digesters. We observed substantial diversification in community composition, with only a few abundant OTUs (e.g. Clostridiales, Anaerolineaceae and Methanosaeta) persistently present across different samples. Similarly, there were high variations in relative abundance of methanogenic archaea and methanogenic genes, which were positively correlated (r2 = 0.530, P

Anaerobic digestion is one of the most successful waste management strategies worldwide, wherein microorganisms play an essential role in reducing organic pollutants and producing renewable energy. However, variations of microbial community in full-scale anaerobic digesters, particularly functional groups relevant to biogas production, remain elusive. Here, we examined microbial community in a year-long monthly time series of 3 full-scale anaerobic digesters. We observed substantial diversification in community composition, with only a few abundant OTUs (e.g. Clostridiales, Anaerolineaceae and Methanosaeta) persistently present across different samples. Similarly, there were high variations in relative abundance of methanogenic archaea and methanogenic genes, which were positively correlated (r2 = 0.530, P

Both fungi and bacteria play essential roles in regulating soil carbon cycling. To predict future carbon stability, it is imperative to understand their responses to environmental changes, which is subject to large uncertainty. As current global warming is causing range shifts toward higher latitudes, we conducted three reciprocal soil transplantation experiments over large transects in 2005 to simulate abrupt climate changes. Six years after soil transplantation, fungal biomass of transplanted soils showed a general pattern of changes from donor sites to destination, which were more obvious in bare fallow soils than in maize cropped soils. Strikingly, fungal community compositions were clustered by sites, demonstrating that fungi of transplanted soils acclimatized to the destination environment. Several fungal taxa displayed sharp changes in relative abundance, including Podospora, Chaetomium, Mortierella and Phialemonium. In contrast, bacterial communities remained largely unchanged. Consistent with the important role of fungi in affecting soil carbon cycling, 8.1%-10.0% of fungal genes encoding carbon-decomposing enzymes were significantly (p

Determining the temporal scaling of biodiversity, typically described as species-time relationships (STRs), in the face of global climate change is a central issue in ecology because it is fundamental to biodiversity preservation and ecosystem management. However, whether and how climate change affects microbial STRs remains unclear, mainly due to the scarcity of long-term experimental data. Here, we examine the STRs and phylogenetic-time relationships (PTRs) of soil bacteria and fungi in a long-term multifactorial global change experiment with warming (+3 °C), half precipitation (-50%), double precipitation (+100%) and clipping (annual plant biomass removal). Soil bacteria and fungi all exhibited strong STRs and PTRs across the 12 experimental conditions. Strikingly, warming accelerated the bacterial and fungal STR and PTR exponents (that is, the w values), yielding significantly (P

Both fungi and bacteria play essential roles in regulating soil carbon cycling. To predict future carbon stability, it is imperative to understand their responses to environmental changes, which is subject to large uncertainty. As current global warming is causing range shifts toward higher latitudes, we conducted three reciprocal soil transplantation experiments over large transects in 2005 to simulate abrupt climate changes. Six years after soil transplantation, fungal biomass of transplanted soils showed a general pattern of changes from donor sites to destination, which were more obvious in bare fallow soils than in maize cropped soils. Strikingly, fungal community compositions were clustered by sites, demonstrating that fungi of transplanted soils acclimatized to the destination environment. Several fungal taxa displayed sharp changes in relative abundance, including Podospora, Chaetomium, Mortierella and Phialemonium. In contrast, bacterial communities remained largely unchanged. Consistent with the important role of fungi in affecting soil carbon cycling, 8.1%-10.0% of fungal genes encoding carbon-decomposing enzymes were significantly (p

Determining the temporal scaling of biodiversity, typically described as species-time relationships (STRs), in the face of global climate change is a central issue in ecology because it is fundamental to biodiversity preservation and ecosystem management. However, whether and how climate change affects microbial STRs remains unclear, mainly due to the scarcity of long-term experimental data. Here, we examine the STRs and phylogenetic-time relationships (PTRs) of soil bacteria and fungi in a long-term multifactorial global change experiment with warming (+3 °C), half precipitation (-50%), double precipitation (+100%) and clipping (annual plant biomass removal). Soil bacteria and fungi all exhibited strong STRs and PTRs across the 12 experimental conditions. Strikingly, warming accelerated the bacterial and fungal STR and PTR exponents (that is, the w values), yielding significantly (P

Tundra ecosystems are typically carbon (C) rich but nitrogen (N) limited. Since biological N2 fixation is the major source of biologically available N, the soil N2-fixing (i.e., diazotrophic) community serves as an essential N supplier to the tundra ecosystem. Recent climate warming has induced deeper permafrost thaw and adversely affected C sequestration, which is modulated by N availability. Therefore, it is crucial to examine the responses of diazotrophic communities to warming across the depths of tundra soils. Herein, we carried out one of the deepest sequencing efforts of nitrogenase gene (nifH) to investigate how 5 years of experimental winter warming affects Alaskan soil diazotrophic community composition and abundance spanning both the organic and mineral layers. Although soil depth had a stronger influence on diazotrophic community composition than warming, warming significantly (P

Tundra ecosystems are typically carbon (C) rich but nitrogen (N) limited. Since biological N2 fixation is the major source of biologically available N, the soil N2-fixing (i.e., diazotrophic) community serves as an essential N supplier to the tundra ecosystem. Recent climate warming has induced deeper permafrost thaw and adversely affected C sequestration, which is modulated by N availability. Therefore, it is crucial to examine the responses of diazotrophic communities to warming across the depths of tundra soils. Herein, we carried out one of the deepest sequencing efforts of nitrogenase gene (nifH) to investigate how 5 years of experimental winter warming affects Alaskan soil diazotrophic community composition and abundance spanning both the organic and mineral layers. Although soil depth had a stronger influence on diazotrophic community composition than warming, warming significantly (P