Climate change alters temporal dynamics of alpine soil microbial functioning and biogeochemical cycling via earlier snowmelt

Soil microbial communities regulate global biogeochemical cycles and respond rapidly to changing environmental conditions. However, understanding how soil microbial communities respond to climate change, and how this influences biogeochemical cycles, remains a major challenge. This is especially pertinent in alpine regions where climate change is taking place at double the rate of the global average, with large reductions in snow cover and earlier spring snowmelt expected as a consequence. Here, we show that spring snowmelt triggers an abrupt transition in the composition of soil microbial communities of alpine grassland that is closely linked to shifts in soil microbial functioning and biogeochemical pools and fluxes. Further, by experimentally manipulating snow cover we show that this abrupt seasonal transition in wide-ranging microbial and biogeochemical soil properties is advanced by earlier snowmelt. Preceding winter conditions did not change the processes that take place during snowmelt. Our findings emphasise the importance of seasonal dynamics for soil microbial communities and the biogeochemical cycles that they regulate. Moreover, our findings suggest that earlier spring snowmelt due to climate change will have far reaching consequences for microbial communities and nutrient cycling in these globally widespread alpine ecosystems.Subject terms: Metagenomics, Climate-change ecology, Microbial ecology, Biogeochemistry, Soil microbiology     

Abundance and taxonomic affiliation of molybdenum transport and utilization genes in Tengchong hot springs,China

The nitrogen, sulfur and carbon cycles all rely on critical microbial transformations that are carried out by enzymes that require molybdenum (Mo) as a cofactor. Despite Mo importance in these biogeochemical cycles, little information exists about microbial Mo utilization in extreme environments where, due to geochemical conditions, bioavailable Mo may be limited. Using metagenomic data from nine hot springs in Tengchong, Yunnan Province, China, which range in temperature from 42°C to 96°C and pH from 2.3 to 9, the effects of pH, temperature and spring geochemistry on the abundance and taxonomic affiliation of genes related to Mo were studied. Dissolved Mo was only detected at sites with circumneutral pH. However, processes and organisms that require Mo were detected at all sites across all temperature and pH gradients. All sites contained xanthine dehydrogenase, formate dehydrogenase, carbon‐monoxide dehydrogenase, nitrate reductase, sulfite oxidase and methionine‐sulfoxide reductase despite different community compositions. This suggests that different microbial communities, resulting from different physicochemical conditions, may be performing similar metabolic functions. Furthermore, the abundance and taxonomic diversity of Mo‐related annotations increased with higher concentrations of Mo. This study shows that despite geochemical conditions that can limit Mo bioavailability, microbes require Mo for a variety of processes.     

Microbial responses to a changing environment: implications for the future functioning of terrestrial ecosystems

In this review, we present a conceptual model which links plant communities and saprotrophic microbial communities through the reciprocal exchange of growth-limiting resources. We discuss the numerous ways human-induced environmental change has directly and indirectly impacted this relationship, and review microbial responses that have occurred to date. We argue that compositional shifts in saprotrophic microbial communities underlie functional responses to environmental change that have ecosystem-level implications. Drawing on a long-term, large-scale, field experiment, we illustrate how and why chronic atmospheric N deposition can alter saprotrophic communities in the soil of a wide-spread sugar maple (Acer saccharum) ecosystem in northeastern North America, resulting in the slowing of plant litter decay, the rapid accumulation of soil organic matter, and the accelerated production and loss of dissolved organic carbon (DOC). Compositional shifts in soil microbial communities, mediated by ecological interactions among soil saprotrophs, appear to lie at the biogeochemical heart of ecosystem response to environmental change.     

Linking Microbial and Ecosystem Ecology Using Ecological Stoichiometry: A Synthesis of Conceptual and Empirical Approaches

Currently, one of the biggest challenges in microbial and ecosystem ecology is to develop conceptual models that organize the growing body of information on environmental microbiology into a clear mechanistic framework with a direct link to ecosystem processes. Doing so will enable development of testable hypotheses to better direct future research and increase understanding of key constraints on biogeochemical networks. Although the understanding of phenotypic and genotypic diversity of microorganisms in the environment is rapidly accumulating, how controls on microbial physiology ultimately affect biogeochemical fluxes remains poorly understood. We propose that insight into constraints on biogeochemical cycles can be achieved by a more rigorous evaluation of microbial community biomass composition within the context of ecological stoichiometry. Multiple recent studies have pointed to microbial biomass stoichiometry as an important determinant of when microorganisms retain or recycle mineral nutrients. We identify the relevant cellular components that most likely drive changes in microbial biomass stoichiometry by defining a conceptual model rooted in ecological stoichiometry. More importantly, we show how X-ray microanalysis (XRMA), nanoscale secondary ion mass spectroscopy (NanoSIMS), Raman microspectroscopy, and in situ hybridization techniques (for example, FISH) can be applied in concert to allow for direct empirical evaluation of the proposed conceptual framework. This approach links an important piece of the ecological literature, ecological stoichiometry, with the molecular front of the microbial revolution, in an attempt to provide new insight into how microbial physiology could constrain ecosystem processes.     

Phylogenetic and Functional Diversity of Microbial Communities Associated with Subsurface Sediments of the Sonora Margin,Guaymas Basin

Subsurface sediments of the Sonora Margin (Guaymas Basin), located in proximity of active cold seep sites were explored. The taxonomic and functional diversity of bacterial and archaeal communities were investigated from 1 to 10 meters below the seafloor. Microbial community structure and abundance and distribution of dominant populations were assessed using complementary molecular approaches (Ribosomal Intergenic Spacer Analysis, 16S rRNA libraries and quantitative PCR with an extensive primers set) and correlated to comprehensive geochemical data. Moreover the metabolic potentials and functional traits of the microbial community were also identified using the GeoChip functional gene microarray and metabolic rates. The active microbial community structure in the Sonora Margin sediments was related to deep subsurface ecosystems (Marine Benthic Groups B and D, Miscellaneous Crenarchaeotal Group, Chloroflexi and Candidate divisions) and remained relatively similar throughout the sediment section, despite defined biogeochemical gradients. However, relative abundances of bacterial and archaeal dominant lineages were significantly correlated with organic carbon quantity and origin. Consistently, metabolic pathways for the degradation and assimilation of this organic carbon as well as genetic potentials for the transformation of detrital organic matters, hydrocarbons and recalcitrant substrates were detected, suggesting that chemoorganotrophic microorganisms may dominate the microbial community of the Sonora Margin subsurface sediments.     

Seasonal hydrologic and geologic forcing drive hot spring geochemistry and microbial biodiversity

Hot springs integrate hydrologic and geologic processes that vary over short- and long-term time scales. However, the influence of temporal hydrologic and geologic change on hot spring biodiversity is unknown. Here, we coordinated near-weekly, cross-seasonal (~140 days) geochemical and microbial community analyses of three widely studied hot springs with local precipitation data in Yellowstone National Park. One spring (‘HFS’) exhibited statistically significant, coupled microbial and geochemical variation across seasons that was associated with recent precipitation patterns. Two other spring communities, ‘CP’ and ‘DS’, exhibited minimal to no variation across seasons. Variability in the seasonal response of springs is attributed to differences in the timing and extent of aquifer recharge with oxidized near-surface water from precipitation. This influx of oxidized water is associated with changes in community composition, and in particular, the abundances of aerobic sulfide-/sulfur-oxidizers that can acidify waters. During sampling, a new spring formed after a period of heavy precipitation and its successional dynamics were also influenced by surface water recharge. Collectively, these results indicate that changes in short-term hydrology associated with precipitation can impact hot spring geochemistry and microbial biodiversity. These results point to potential susceptibility of certain hot springs and their biodiversity to sustained, longer-term hydrologic changes.     

Phage community dynamics in hot springs

In extreme thermal environments such as hot springs, phages are the only known microbial predators. Here we present the first study of prokaryotic and phage community dynamics in these environments. Phages were abundant in hot springs, reaching concentrations of a million viruses per milliliter. Hot spring phage particles were resistant to shifts to lower temperatures, possibly facilitating DNA transfer out of these extreme environments. The phages were actively produced, with a population turnover time of 1 to 2 days. Phage-mediated microbial mortality was significant, making phage lysis an important component of hot spring microbial food webs. Together, these results show that phages exert an important influence on microbial community structure and energy flow in extreme thermal environments.     

Phage Community Dynamics in Hot Springs

In extreme thermal environments such as hot springs, phages are the only known microbial predators. Here we present the first study of prokaryotic and phage community dynamics in these environments. Phages were abundant in hot springs, reaching concentrations of a million viruses per milliliter. Hot spring phage particles were resistant to shifts to lower temperatures, possibly facilitating DNA transfer out of these extreme environments. The phages were actively produced, with a population turnover time of 1 to 2 days. Phage-mediated microbial mortality was significant, making phage lysis an important component of hot spring microbial food webs. Together, these results show that phages exert an important influence on microbial community structure and energy flow in extreme thermal environments.     

Functional gene diversity of soil microbial communities from five oil-contaminated fields in China

To compare microbial functional diversity in different oil-contaminated fields and to know the effects of oil contaminant and environmental factors, soil samples were taken from typical oil-contaminated fields located in five geographic regions of China. GeoChip, a high-throughput functional gene array, was used to evaluate the microbial functional genes involved in contaminant degradation and in other major biogeochemical/metabolic processes. Our results indicated that the overall microbial community structures were distinct in each oil-contaminated field, and samples were clustered by geographic locations. The organic contaminant degradation genes were most abundant in all samples and presented a similar pattern under oil contaminant stress among the five fields. In addition, alkane and aromatic hydrocarbon degradation genes such as monooxygenase and dioxygenase were detected in high abundance in the oil-contaminated fields. Canonical correspondence analysis indicated that the microbial functional patterns were highly correlated to the local environmental variables, such as oil contaminant concentration, nitrogen and phosphorus contents, salt and pH. Finally, a total of 59% of microbial community variation from GeoChip data can be explained by oil contamination, geographic location and soil geochemical parameters. This study provided insights into the in situ microbial functional structures in oil-contaminated fields and discerned the linkages between microbial communities and environmental variables, which is important to the application of bioremediation in oil-contaminated sites.     

湖泊硫循环微生物研究进展

湖泊是响应气候和环境变化的关键生态系统,是研究元素(如碳、氮和硫等)生物地球化学循环的热点环境。湖泊(尤其咸盐湖)具有硫酸盐含量高且含硫化合物种类丰富的特点,因而湖泊中硫元素生物地球化学循环过程非常活跃。微生物是驱动湖泊硫循环的重要推手。因此,研究湖泊中微生物参与的硫元素生物地球化学循环过程以及相关微生物类群构成,对于深入探索微生物在湖泊生态系统中的作用具有重要意义。本文综述了湖泊中驱动硫循环的微生物(硫氧化菌和硫酸盐还原菌)种群多样性、功能基因、代谢途径、硫氧化/硫酸盐还原速率及其对环境条件变化响应等方面的研究现状,并对未来湖泊微生物驱动的硫循环研究方向进行了展望。     

Applying population and community ecology theory to advance understanding of belowground biogeochemistry

Approaches to quantifying and predicting soil biogeochemical cycles mostly consider microbial biomass and community composition as products of the abiotic environment. Current numerical approaches then primarily emphasise the importance of microbe–environment interactions and physiology as controls on biogeochemical cycles. Decidedly less attention has been paid to understanding control exerted by community dynamics and biotic interactions. Yet a rich literature of theoretical and empirical contributions highlights the importance of considering how variation in microbial population ecology, especially biotic interactions, is related to variation in key biogeochemical processes like soil carbon formation. We demonstrate how a population and community ecology perspective can be used to (1) understand the impact of microbial communities on biogeochemical cycles and (2) reframe current theory and models to include more detailed microbial ecology. Through a series of simulations we illustrate how density dependence and key biotic interactions, such as competition and predation, can determine the degree to which microbes regulate soil biogeochemical cycles. The ecological perspective and model simulations we present lay the foundation for developing empirical research and complementary models that explore the diversity of ecological mechanisms that operate in microbial communities to regulate biogeochemical processes.     

热泉微生物驱动的氮循环研究进展及展望

热泉微生物是驱动热泉氮(N)循环的主导力量,开展热泉生态系统中驱动氮循环微生物种群构成及其与环境响应的研究,对于探索热泉中氮的生物地球化学循环、生命进化、生物修复等方面都具有重要的理论和应用价值。本文综合阐述了热泉生态系统驱动氮循环的功能微生物(如固氮菌、氨氧化菌、厌氧氨氧化菌、反硝化菌、异化硝酸盐还原菌)在系统发育学上的分布、功能基因的相对丰度、活性及其与环境因子(如温度、pH)的相关性等方面的研究现状和亟待解决的问题。并展望了热泉生境中驱动氮循环微生物未来的研究方向。     

Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles – upscaling an aggregate biophysical model

Microbial communities inhabiting soil aggregates dynamically adjust their activity and composition in response to variations in hydration and other external conditions. These rapid dynamics shape signatures of biogeochemical activity and gas fluxes emitted from soil profiles. Recent mechanistic models of microbial processes in unsaturated aggregate‐like pore networks revealed a highly dynamic interplay between oxic and anoxic microsites jointly shaped by hydration conditions and by aerobic and anaerobic microbial community abundance and self‐organization. The spatial extent of anoxic niches (hotspots) flicker in time (hot moments) and support substantial anaerobic microbial activity even in aerated soil profiles. We employed an individual‐based model for microbial community life in soil aggregate assemblies represented by 3D angular pore networks. Model aggregates of different sizes were subjected to variable water, carbon and oxygen contents that varied with soil depth as boundary conditions. The study integrates microbial activity within aggregates of different sizes and soil depth to obtain estimates of biogeochemical fluxes from the soil profile. The results quantify impacts of dynamic shifts in microbial community composition on CO₂ and N₂O production rates in soil profiles in good agreement with experimental data. Aggregate size distribution and the shape of resource profiles in a soil determine how hydration dynamics shape denitrification and carbon utilization rates. Results from the mechanistic model for microbial activity in aggregates of different sizes were used to derive parameters for analytical representation of soil biogeochemical processes across large scales of practical interest for hydrological and climate models.     

Burning Fire-Prone Mediterranean Shrublands: Immediate Changes in Soil Microbial Community Structure and Ecosystem Functions

Wildfires subject soil microbes to extreme temperatures and modify their physical and chemical habitat. This might immediately alter their community structure and ecosystem functions. We burned a fire-prone shrubland under controlled conditions to investigate (1) the fire-induced changes in the community structure of soil archaea, bacteria and fungi by analysing 16S or 18S rRNA gene amplicons separated through denaturing gradient gel electrophoresis; (2) the physical and chemical variables determining the immediate shifts in the microbial community structure; and (3) the microbial drivers of the change in ecosystem functions related to biogeochemical cycling. Prokaryotes and eukaryotes were structured by the local environment in pre-fire soils. Fire caused a significant shift in the microbial community structure, biomass C, respiration and soil hydrolases. One-day changes in bacterial and fungal community structure correlated to the rise in total organic C and NO(3)(-)-N caused by the combustion of plant residues. In the following week, bacterial communities shifted further forced by desiccation and increasing concentrations of macronutrients. Shifts in archaeal community structure were unrelated to any of the 18 environmental variables measured. Fire-induced changes in the community structure of bacteria, rather than archaea or fungi, were correlated to the enhanced microbial biomass, CO(2) production and hydrolysis of C and P organics. This is the first report on the combined effects of fire on the three biological domains in soils. We concluded that immediately after fire the biogeochemical cycling in Mediterranean shrublands becomes less conservative through the increased microbial biomass, activity and changes in the bacterial community structure.     

Microbial minorities modulate methane consumption through niche partitioning

Microbes catalyze all major geochemical cycles on earth. However, the role of microbial traits and community composition in biogeochemical cycles is still poorly understood mainly due to the inability to assess the community members that are actually performing biogeochemical conversions in complex environmental samples. Here we applied a polyphasic approach to assess the role of microbial community composition in modulating methane emission from a riparian floodplain. We show that the dynamics and intensity of methane consumption in riparian wetlands coincide with relative abundance and activity of specific subgroups of methane-oxidizing bacteria (MOB), which can be considered as a minor component of the microbial community in this ecosystem. Microarray-based community composition analyses demonstrated linear relationships of MOB diversity parameters and in vitro methane consumption. Incubations using intact cores in combination with stable isotope labeling of lipids and proteins corroborated the correlative evidence from in vitro incubations demonstrating γ-proteobacterial MOB subgroups to be responsible for methane oxidation. The results obtained within the riparian flooding gradient collectively demonstrate that niche partitioning of MOB within a community comprised of a very limited amount of active species modulates methane consumption and emission from this wetland. The implications of the results obtained for biodiversity–ecosystem functioning are discussed with special reference to the role of spatial and temporal heterogeneity and functional redundancy.     

Archaeal and bacterial communities in geochemically diverse hot springs of Yellowstone National Park, USA

Microbiological and geochemical surveys were conducted at three hot springs (Obsidian Pool, Sylvan Spring, and ‘Bison Pool’) in Yellowstone National Park (Wyoming, USA). Microbial community structure was investigated by polymerase chain reaction (PCR) amplification of 16S rRNA gene sequences from DNA extracted from sediments of each hot spring, followed by molecular cloning. Both bacterial and archaeal DNA was retrieved from all samples. No Euryarchaea were found, but diverse Crenarchaea exist in all three pools, particularly affiliating with deep‐branching, but uncultivated organisms. In addition, cloned DNA affiliating with the Desulphurococcales and Thermoproteales was identified, but the distribution of taxa differs in each hot spring. The bacterial community at all three locations is dominated by members of the Aquificales and Thermodesulfobacteriales, indicating that the ‘knallgas’ reaction (aerobic hydrogen oxidation) may be a central metabolism in these ecosystems. To provide geochemical context for the microbial community structures, energy‐yields for a number of chemolithoautotrophic reactions are provided for >80 sampling sites in Yellowstone, including Obsidian Pool, Sylvan Spring, and ‘Bison Pool’. This energy profile shows that the knallgas reaction is just one of many exergonic reactions in the Yellowstone hot springs, that energy‐yields for certain reactions can vary substantially from one site to the next, and that few of the demonstrated exergonic reactions are known to support microbial metabolism.     

Seasonal and spatial variations in microbial community structure and diversity in the acid stream draining across an ongoing surface mining site

This study examined the microbial community in an acidic stream draining across the Yun-Fu pyrite mine (Guangdong, China), where extremely acidic mine water is a persistent feature due to the intensive surface mining activities. Analysis of terminal restriction fragment length polymorphism (TRFLP) of 16S rRNA gene sequences showed that microbial populations varied spatially and seasonally and correlated with geochemical and physical conditions. After the stream moves from underground to the surface, the microbial community in the acidic water rapidly evolves into a distinct community close to that in the downstream storage pond. Comparisons of TRFLP peaks with sequenced clone libraries indicated that bacteria related to the recently isolated iron-oxidizer Ferrovum myxofaciens dominated the acidophilic community throughout the year except for the samples collected in spring from the storage pond, where Ferroplasma acidiphilum -like archaea represented the most abundant group. Acidithiobacillus ferrooxidans -affiliated organisms increased along the acid stream and remained common over the year, whereas Leptospirillum ferrooxidans -like bacteria were negligible or even not detected in the analyzed samples. The data indicate that changes in environmental conditions are accompanied by significant shifts in community structure of the prokaryotic assemblages at this opencast mining site.     

Influence of Seasonal and Geochemical Changes on the Geomicrobiology of an Iron Carbonate Mineral Water Spring

Fuschna Spring in the Swiss Alps (Engadin region) is a bicarbonate iron(II)-rich, pH-neutral mineral water spring that is dominated visually by dark green microbial mats at the side of the flow channel and orange iron(III) (oxyhydr)oxides in the flow channel. Gradients of O₂, dissolved iron(II), and bicarbonate establish in the water. Our goals were to identify the dominating biogeochemical processes and to determine to which extent changing geochemical conditions along the flow path and seasonal changes influence mineral identity, crystallinity, and microbial diversity. Geochemical analysis showed microoxic water at the spring outlet which became fully oxygenated within 2.3 m downstream. X-ray diffraction and Mössbauer spectroscopy revealed calcite (CaCO₃) and ferrihydrite [Fe(OH)₃] to be the dominant minerals which increased in crystallinity with increasing distance from the spring outlet. Denaturing gradient gel electrophoresis banding pattern cluster analysis revealed that the microbial community composition shifted mainly with seasons and to a lesser extent along the flow path. 16S rRNA gene sequence analysis showed that microbial communities differ between the flow channel and the flanking microbial mat. Microbial community analysis in combination with most-probable-number analyses and quantitative PCR (qPCR) showed that the mat was dominated by cyanobacteria and the channel was dominated by microaerophilic Fe(II) oxidizers (1.97 × 10⁷ ± 4.36 × 10⁶ 16S rRNA gene copies g⁻¹ using Gallionella-specific qPCR primers), while high numbers of Fe(III) reducers (10⁹ cells/g) were identified in both the mat and the flow channel. Phototrophic and nitrate-reducing Fe(II) oxidizers were present as well, although in lower numbers (10³ to 10⁴ cells/g). In summary, our data suggest that mainly seasonal changes caused microbial community shifts, while geochemical gradients along the flow path influenced mineral crystallinity.     

Diversity and potential biogeochemical impacts of viruses in bulk and rhizosphere soils

Viruses can affect microbial dynamics, metabolism and biogeochemical cycles in aquatic ecosystems. However, viral diversity and functions in agricultural soils are poorly known, especially in the rhizosphere. We used virome analysis of eight rhizosphere and bulk soils to study viral diversity and potential biogeochemical impacts in an agro-ecosystem. The order Caudovirales was the predominant viral type in agricultural soils, with Siphoviridae being the most abundant family. Phylogenetic analysis of the terminase large subunit of Caudovirales identified high viral diversity and three novel groups. Viral community composition differed significantly between bulk and rhizosphere soils. Soil pH was the main environmental driver of the viral community structure. Remarkably, abundant auxiliary carbohydrate-active enzyme (CAZyme) genes were detected in viromes, including glycoside hydrolases, carbohydrate esterases and carbohydrate-binding modules. These results demonstrate that virus-encoded putative auxiliary metabolic genes or metabolic genes that may change bacterial metabolism and indirectly contribute to biogeochemical cycling, especially carbon cycling, in agricultural soil.