Temporal and spatial constraints on community assembly during microbial colonization of wood in seawater

Wood falls on the ocean floor form chemosynthetic ecosystems that remain poorly studied compared with features such as hydrothermal vents or whale falls. In particular, the microbes forming the base of this unique ecosystem are not well characterized and the ecology of communities is not known. Here we use wood as a model to study microorganisms that establish and maintain a chemosynthetic ecosystem. We conducted both aquaria and in situ deep-sea experiments to test how different environmental constraints structure the assembly of bacterial, archaeal and fungal communities. We also measured changes in wood lipid concentrations and monitored sulfide production as a way to detect potential microbial activity. We show that wood falls are dynamic ecosystems with high spatial and temporal community turnover, and that the patterns of microbial colonization change depending on the scale of observation. The most illustrative example was the difference observed between pine and oak wood community dynamics. In pine, communities changed spatially, with strong differences in community composition between wood microhabitats, whereas in oak, communities changed more significantly with time of incubation. Changes in community assembly were reflected by changes in phylogenetic diversity that could be interpreted as shifts between assemblies ruled by species sorting to assemblies structured by competitive exclusion. These ecological interactions followed the dynamics of the potential microbial metabolisms accompanying wood degradation in the sea. Our work showed that wood is a good model for creating and manipulating chemosynthetic ecosystems in the laboratory, and attracting not only typical chemosynthetic microbes but also emblematic macrofaunal species.     

Environmental and biotic drivers of soil microbial β‐diversity across spatial and phylogenetic scales

Soil microbial communities play a key role in ecosystem functioning but still little is known about the processes that determine their turnover (β‐diversity) along ecological gradients. Here, we characterize soil microbial β‐diversity at two spatial scales and at multiple phylogenetic grains to ask how archaeal, bacterial and fungal communities are shaped by abiotic processes and biotic interactions with plants. We characterized microbial and plant communities using DNA metabarcoding of soil samples distributed across and within eighteen plots along an elevation gradient in the French Alps. The recovered taxa were placed onto phylogenies to estimate microbial and plant β‐diversity at different phylogenetic grains (i.e. resolution). We then modeled microbial β‐diversities with respect to plant β‐diversities and environmental dissimilarities across plots (landscape scale) and with respect to plant β‐diversities and spatial distances within plots (plot scale). At the landscape scale, fungal and archaeal β‐diversities were mostly related to plant β‐diversity, while bacterial β‐diversities were mostly related to environmental dissimilarities. At the plot scale, we detected a modest covariation of bacterial and fungal β‐diversities with plant β‐diversity; as well as a distance–decay relationship that suggested the influence of ecological drift on microbial communities. In addition, the covariation between fungal and plant β‐diversity at the plot scale was highest at fine or intermediate phylogenetic grains hinting that biotic interactions between those clades depends on early‐evolved traits. Altogether, we show how multiple ecological processes determine soil microbial community assembly at different spatial scales and how the strength of these processes change among microbial clades. In addition, we emphasized the imprint of microbial and plant evolutionary history on today's microbial community structure.     

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.     

根际微生物组组装与植物健康

土壤微生物拥有高度多样化的群落结构,其通过与植物发生复杂的相互作用影响植物健康,也被称为植物的第二基因组。最近研究表明植物能通过改变根际分泌物的组成影响根际微生物群落的组装,反之,根际微生物群落组成的改变能够通过影响植物营养吸收和抵御生物及非生物胁迫的能力影响植物健康。除此之外,农艺管理也是影响土壤微生物群落组装方式的重要因素。但到目前为止,根际微生物与宿主植物及土壤微生物之间互作机制的研究尚不清楚。本文将从农艺管理和宿主植物对微生物群落组装的影响及根际微生物组对植物健康的影响进行总结,为增加作物产量提供机会。     

Do biotic interactions modulate ecosystem functioning along stress gradients? Insights from semi-arid plant and biological soil crust communities

Climate change will exacerbate the degree of abiotic stress experienced by semi-arid ecosystems. While abiotic stress profoundly affects biotic interactions, their potential role as modulators of ecosystem responses to climate change is largely unknown. Using plants and biological soil crusts, we tested the relative importance of facilitative–competitive interactions and other community attributes (cover, species richness and species evenness) as drivers of ecosystem functioning along stress gradients in semi-arid Mediterranean ecosystems. Biotic interactions shifted from facilitation to competition along stress gradients driven by water availability and temperature. These changes were, however, dependent on the spatial scale and the community considered. We found little evidence to suggest that biotic interactions are a major direct influence upon indicators of ecosystem functioning (soil respiration, organic carbon, water-holding capacity, compaction and the activity of enzymes related to the carbon, nitrogen and phosphorus cycles) along stress gradients. However, attributes such as cover and species richness showed a direct effect on ecosystem functioning. Our results do not agree with predictions emphasizing that the importance of plant–plant interactions will be increased under climate change in dry environments, and indicate that reductions in the cover of plant and biological soil crust communities will negatively impact ecosystems under future climatic conditions.     

Key Edaphic Properties Largely Explain Temporal and Geographic Variation in Soil Microbial Communities across Four Biomes

Soil microbial communities play a critical role in nutrient transformation and storage in all ecosystems. Quantifying the seasonal and long-term temporal extent of genetic and functional variation of soil microorganisms in response to biotic and abiotic changes within and across ecosystems will inform our understanding of the effect of climate change on these processes. We examined spatial and seasonal variation in microbial communities based on 16S rRNA gene sequencing and phospholipid fatty acid (PLFA) composition across four biomes: a tropical broadleaf forest (Hawaii), taiga (Alaska), semiarid grassland-shrubland (Utah), and a subtropical coniferous forest (Florida). In this study, we used a team-based instructional approach leveraging the iPlant Collaborative to examine publicly available National Ecological Observatory Network (NEON) 16S gene and PLFA measurements that quantify microbial diversity, composition, and growth. Both profiling techniques revealed that microbial communities grouped strongly by ecosystem and were predominately influenced by three edaphic factors: pH, soil water content, and cation exchange capacity. Temporal variability of microbial communities differed by profiling technique; 16S-based community measurements showed significant temporal variability only in the subtropical coniferous forest communities, specifically through changes within subgroups of Acidobacteria. Conversely, PLFA-based community measurements showed seasonal shifts in taiga and tropical broadleaf forest systems. These differences may be due to the premise that 16S-based measurements are predominantly influenced by large shifts in the abiotic soil environment, while PLFA-based analyses reflect the metabolically active fraction of the microbial community, which is more sensitive to local disturbances and biotic interactions. To address the technical issue of the response of soil microbial communities to sample storage temperature, we compared 16S-based community structure in soils stored at -80°C and -20°C and found no significant differences in community composition based on storage temperature. Free, open access datasets and data sharing platforms are powerful tools for integrating research and teaching in undergraduate and graduate student classrooms. They are a valuable resource for fostering interdisciplinary collaborations, testing ecological theory, model development and validation, and generating novel hypotheses. Training in data analysis and interpretation of large datasets in university classrooms through project-based learning improves the learning experience for students and enables their use of these significant resources throughout their careers.     

Fungal-Fungal Associations Affect the Assembly of Endophyte Communities in Maize (Zea mays)

Many factors can affect the assembly of communities, ranging from species pools to habitat effects to interspecific interactions. In microbial communities, the predominant focus has been on the well-touted ability of microbes to disperse and the environment acting as a selective filter to determine which species are present. In this study, we investigated the role of biotic interactions (e.g., competition, facilitation) in fungal endophyte community assembly by examining endophyte species co-occurrences within communities using null models. We used recombinant inbred lines (genotypes) of maize (Zea mays) to examine community assembly at multiple habitat levels, at the individual plant and host genotype levels. Both culture-dependent and culture-independent approaches were used to assess endophyte communities. Communities were analyzed using the complete fungal operational taxonomic unit (OTU) dataset or only the dominant (most abundant) OTUs in order to ascertain whether species co-occurrences were different for dominant members compared to when all members were included. In the culture-dependent approach, we found that for both datasets, OTUs co-occurred on maize genotypes more frequently than expected under the null model of random species co-occurrences. In the culture-independent approach, we found that OTUs negatively co-occurred at the individual plant level but were not significantly different from random at the genotype level for either the dominant or complete datasets. Our results showed that interspecific interactions can affect endophyte community assembly, but the effects can be complex and depend on host habitat level. To our knowledge, this is the first study to examine endophyte community assembly in the same host species at multiple habitat levels. Understanding the processes and mechanisms that shape microbial communities will provide important insights into microbial community structure and the maintenance of microbial biodiversity.     

Distinct patterns of soil bacterial and fungal community assemblages in subtropical forest ecosystems under warming

Climate change globally affects soil microbial community assembly across ecosystems. However, little is known about the impact of warming on the structure of soil microbial communities or underlying mechanisms that shape microbial community composition in subtropical forest ecosystems. To address this gap, we utilized natural variation in temperature via an altitudinal gradient to simulate ecosystem warming. After 6 years, microbial co-occurrence network complexity increased with warming, and changes in their taxonomic composition were asynchronous, likely due to contrasting community assembly processes. We found that while stochastic processes were drivers of bacterial community composition, warming led to a shift from stochastic to deterministic drivers in dry season. Structural equation modelling highlighted that soil temperature and water content positively influenced soil microbial communities during dry season and negatively during wet season. These results facilitate our understanding of the response of soil microbial communities to climate warming and may improve predictions of ecosystem function of soil microbes in subtropical forests.     

Microbial resistance and resilience in response to environmental changes under the higher intensity of human activities than global average level

With the increasing intensity of global human activities, the ecosystem function, which is supported by the microbial community, will be dramatically changed and impaired. To investigate microbial resistance and resilience of microbial communities to human activities, we chose two typical types of human disturbances, urbanization, and reclamation under the higher intensity of human activities than the global average level. We examined microbial traits, including the abundance, diversity, phylogeny, and co‐occurrence interactions in soil microbial communities, together with the nitrification activities observed in the subtropical coastal ecosystem of the Pearl River Estuary and in soil microcosm experiments. Microbial communities were less resistant to the environmental changes caused by urbanization than to those caused by reclamation, which was significantly reflected in the nitrogen and/or carbon‐related patterns. However, most of the microbial traits could be recovered almost to the original level without significant differences in the microcosm after 40 days of incubation. The co‐occurrence interactions between nitrifiers and other microbial communities were dramatically changed and could not be completely recovered, but this change did not affect their nitrification activities for balancing the ammonium in the soil to the original level during the recovery stage, suggesting that the interactions between microbial communities might have fewer effects on their activities than previously thought. This study quantitatively demonstrated that microbial communities as a whole can recover to a status similar to the original state in a short time after the removal of stress at a large ecosystem scale even under the higher intensity of human activities than global average level in coastal ecosystems, which implied a strong recovery capacity of soil microbial community even after intense human disturbance.     

Biogeographic responses and niche occupancy of microbial communities following long-term land-use change

Understanding the effects of forest-to-agriculture conversion on microbial diversity has been a major goal in soil ecological studies. However, linking community assembly to the ruling ecological processes at local and regional scales remains challenging. Here, we evaluated bacterial community assembly patterns and the ecological processes governing niche specialization in a gradient of geography, seasonality, and land-use change, totaling 324 soil samples, 43 habitat characteristics (abiotic factors), and 16 metabolic and co-occurrence patterns (biotic factors), in the Brazilian Atlantic Rainforest, a subtropical biome recognized as one the world’s largest and most threatened hotspots of biodiversity. Pairwise beta diversities were lower in pastures than in forest and no-till soils. Pasture communities showed a predominantly neutral model, regarding stochastic processes, with moderate dispersion, leading to biotic homogenization. Most no-till and forest microbial communities followed a niche-based model, with low rates of dispersal and weak homogenizing selection, indicating niche specialization or variable selection. Historical and evolutionary contingencies, as represented by soil type, season, and dispersal limitation were the main drivers of microbial assembly and processes at the local scale, markedly correlated with the occurrence of endemic microbes. Our results indicate that the patterns of assembly and their governing processes are dependent on the niche occupancy of the taxa evaluated (generalists or specialists). They are also more correlated with historical and evolutionary contingencies and the interactions among taxa (i.e., co-occurrence patterns) than the land-use change itself.

     

Relating microbial community structure to functioning in forest soil organic carbon transformation and turnover

Forest soils store vast amounts of terrestrial carbon, but we are still limited in mechanistic understanding on how soil organic carbon (SOC) stabilization or turnover is controlled by biotic and abiotic factors in forest ecosystems. We used phospholipid fatty acids (PLFAs) as biomarker to study soil microbial community structure and measured activities of five extracellular enzymes involved in the degradation of cellulose (i.e., β‐1,4‐glucosidase and cellobiohydrolase), chitin (i.e., β‐1,4‐N‐acetylglucosaminidase), and lignin (i.e., phenol oxidase and peroxidase) as indicators of soil microbial functioning in carbon transformation or turnover across varying biotic and abiotic conditions in a typical temperate forest ecosystem in central China. Redundancy analysis (RDA) was performed to determine the interrelationship between individual PFLAs and biotic and abiotic site factors as well as the linkage between soil microbial structure and function. Path analysis was further conducted to examine the controls of site factors on soil microbial community structure and the regulatory pathway of changes in SOC relating to microbial community structure and function. We found that soil microbial community structure is strongly influenced by water, temperature, SOC, fine root mass, clay content, and C/N ratio in soils and that the relative abundance of Gram‐negative bacteria, saprophytic fungi, and actinomycetes explained most of the variations in the specific activities of soil enzymes involved in SOC transformation or turnover. The abundance of soil bacterial communities is strongly linked with the extracellular enzymes involved in carbon transformation, whereas the abundance of saprophytic fungi is associated with activities of extracellular enzymes driving carbon oxidation. Findings in this study demonstrate the complex interactions and linkage among plant traits, microenvironment, and soil physiochemical properties in affecting SOC via microbial regulations.     

Plant community and soil conditions individually affect soil microbial community assembly in experimental mesocosms

Soils harbor large, diverse microbial communities critical for local and global ecosystem functioning that are controlled by multiple and poorly understood processes. In particular, while there is observational evidence of relationships between both biotic and abiotic conditions and microbial composition and diversity, there have been few experimental tests to determine the relative importance of these two sets of factors at local scales. Here, we report the results of a fully factorial experiment manipulating soil conditions and plant cover on old‐field mesocosms across a latitudinal gradient. The largest contributor to beta diversity was site‐to‐site variation, but, having corrected for that, we observed significant effects of both plant and soil treatments on microbial composition. Separate phyla were associated with each treatment type, and no interactions between soil and plant treatment were observed. Individual soil characteristics and biotic parameters were also associated with overall beta‐diversity patterns and phyla abundance. In contrast, soil microbial diversity was only associated with site and not experimental treatment. Overall, plant community treatment explained more variation than soil treatment, a result not previously appreciated because it is difficult to dissociate plant community composition and soil conditions in observational studies across gradients. This work highlights the need for more nuanced, multifactorial experiments in microbial ecology and in particular indicates a greater focus on relationships between plant composition and microbial composition during community assembly.     

Incorporating phylogenetic metrics to microbial co‐occurrence networks based on amplicon sequences to discern community assembly processes

Co‐occurrence network analysis based on amplicon sequences is increasingly used to study microbial communities. Patterns of co‐existence or mutual exclusion between pairs of taxa are often interpreted as reflecting positive or negative biological interactions. However, other assembly processes can underlie these patterns, including species failure to reach distant areas (dispersal limitation) and tolerate local environmental conditions (habitat filtering). We provide a tool to quantify the relative contribution of community assembly processes to microbial co‐occurrence patterns, which we applied to explore soil bacterial communities in two dry ecosystems. First, we sequenced a bacterial phylogenetic marker in soils collected across multiple plots. Second, we inferred co‐occurrence networks to identify pairs of significantly associated taxa, either co‐existing more (aggregated) or less often (segregated) than expected at random. Third, we assigned assembly processes to each pair: patterns explained based on spatial or environmental distance were ascribed to dispersal limitation (2%–4%) or habitat filtering (55%–77%), and the remaining to biological interactions. Finally, we calculated the phylogenetic distance between taxon pairs to test theoretical expectations on the linkages between phylogenetic patterns and assembly processes. Aggregated pairs were more closely related than segregated pairs. Furthermore, habitat‐filtered aggregated pairs were closer relatives than those assigned to positive interactions, consistent with phylogenetic niche conservatism and cooperativism among distantly related taxa. Negative interactions resulted in equivocal phylogenetic signatures, probably because different competitive processes leave opposing signals. We show that microbial co‐occurrence networks mainly reflect environmental tolerances and propose that incorporating measures of phylogenetic relatedness to networks might help elucidate ecologically meaningful patterns.     

Biotic interactions hold the key to understanding metacommunity organisation

Biotic interactions are fundamental drivers governing biodiversity locally, yet their effects on geographical variation in community composition (i.e. incidence-based) and community structure (i.e. abundance-based) at regional scales remain controversial. Ecologists have only recently started to integrate different types of biotic interactions into community assembly in a spatial context, a theme that merits further empirical quantification. Here, we applied partial correlation networks to infer the strength of spatial dependencies between pairs of organismal groups and mapped the imprints of biotic interactions on the assembly of pond metacommunities. To do this, we used a comprehensive empirical dataset from Mediterranean landscapes and adopted the perspective that community assembly is best represented as a network of interacting organismal groups. Our results revealed that the co-variation among the beta diversities of multiple organismal groups is primarily driven by biotic interactions and, to a lesser extent, by the abiotic environment. These results suggest that ignoring biotic interactions may undermine our understanding of assembly mechanisms in spatially extensive areas and decrease the accuracy and performance of predictive models. We further found strong spatial dependencies in our analyses which can be interpreted as functional relationships among several pairs of organismal groups (e.g. macrophytes–macroinvertebrates, fish–zooplankton). Perhaps more importantly, our results support the notion that biotic interactions make crucial contributions to the species sorting paradigm of metacommunity theory and raise the question of whether these biologically-driven signals have been equally underappreciated in other aquatic and terrestrial ecosystems. Although more research is still required to empirically capture the importance of biotic interactions across ecosystems and at different spatial resolutions and extents, our findings may allow decision makers to better foresee the main consequences of human-driven impacts on inland waters, particularly those associated with the addition or removal of key species.     

Interactive effects of warming and invertebrate grazing on the outcomes of competitive fungal interactions

Saprotrophic fungal community composition, determined by the outcomes of competitive mycelial interactions, represents a key determinant of woodland carbon and nutrient cycling. Atmospheric warming is predicted to drive changes in fungal community composition. Grazing by invertebrates can also exert selective pressures on fungal communities and alter the outcome of competitive fungal interactions; their potential to do so is determined by grazing intensity. Temperature regulates the abundance of soil collembola, but it remains unclear whether this will alter the top-down determination of fungal community composition. We use soil microcosms to explore the direct (via effects on interacting fungi) and indirect (by influencing top-down grazing pressures) effects of a 3 °C temperature increase on the outcomes of competitive interactions between cord-forming basidiomycete fungi. By differentially affecting the fungal growth rates, warming reversed the outcomes of specific competitive interactions. Collembola populations also increased at elevated temperature, and these larger, more active, populations exerted stronger grazing pressures. Consequently, grazing mitigated the effects of temperature on these interactions, restoring fungal communities to those recorded at ambient temperature. The interactive effects of biotic and abiotic factors are a key in determining the functional and ecological responses of microbial communities to climate change.     

The root microbiome: Community assembly and its contributions to plant fitness

The root microbiome refers to the community of microbes living in association with a plant's roots, and includes mutualists, pathogens, and commensals. Here we focus on recent advances in the study of root commensal community which is the major research object of microbiome-related researches. With the rapid development of new technologies, plant–commensal interactions can be explored with unprecedented breadth and depth. Both the soil environment and the host plant drive commensal community assembly. The bulk soil is the seed bank of potential commensals, and plants use root exudates and immune responses to build healthy microbial communities from the available microbes. The plant microbiome extends the functional system of plants by participating in a variety of processes, including nutrient absorption, growth promotion, and resistance to biotic and abiotic stresses. Plants and their microbiomes have evolved adaptation strategies over time. However, there is still a huge gap in our understanding of the regulatory mechanisms of plant–commensal interactions. In this review, we summarize recent research on the assembly of root microbial communities and the effects of these communities on plant growth and development, and look at the prospects for promoting sustainable agricultural development through the study of the root microbiome.     

Revisiting the Dilution Procedure Used To Manipulate Microbial Biodiversity in Terrestrial Systems

It is hard to assess experimentally the importance of microbial diversity in soil for the functioning of terrestrial ecosystems. An approach that is often used to make such assessment is the so-called dilution method. This method is based on the assumption that the biodiversity of the microbial community is reduced after dilution of a soil suspension and that the reduced diversity persists after incubation of more or less diluted inocula in soil. However, little is known about how the communities develop in soil after inoculation. In this study, serial dilutions of a soil suspension were made and reinoculated into the original soil previously sterilized by gamma irradiation. We determined the structure of the microbial communities in the suspensions and in the inoculated soils using 454-pyrosequencing of 16S rRNA genes. Upon dilution, several diversity indices showed that, indeed, the diversity of the bacterial communities in the suspensions decreased dramatically, with Proteobacteria as the dominant phylum of bacteria detected in all dilutions. The structure of the microbial community was changed considerably in soil, with Proteobacteria, Bacteroidetes, and Verrucomicrobia as the dominant groups in most diluted samples, indicating the importance of soil-related mechanisms operating in the assembly of the communities. We found unique operational taxonomic units (OTUs) even in the highest dilution in both the suspensions and the incubated soil samples. We conclude that the dilution approach reduces the diversity of microbial communities in soil samples but that it does not allow accurate predictions of the community assemblage during incubation of (diluted) suspensions in soil.     

Competition and habitat filtering jointly explain phylogenetic structure of soil bacterial communities across elevational gradients

The importance of assembly processes in shaping biological communities is poorly understood, especially for microbes. Here, we report on the forces that structure soil bacterial communities along a 2000 m elevational gradient. We characterized the relative importance of habitat filtering and competition on phylogenetic structure and turnover in bacterial communities. Bacterial communities exhibited a phylogenetically clustered pattern and were more clustered with increasing elevation. Biotic factors (i.e., relative abundance of dominant bacterial lineages) appeared to be most important to the degree of clustering, evidencing the role of the competitive ability of entire clades in shaping the communities. Phylogenetic turnover showed the greatest correlation to elevation. After controlling the elevation, biotic factors showed greater correlation to phylogenetic turnover than all the habitat variables (i.e., climate, soil and vegetation). Structural equation modelling also identified that elevation and soil organic matter exerted indirect effects on phylogenetic diversity and turnover by determining the dominance of microbial competitors. Our results suggest that competition among bacterial taxa induced by soil carbon contributes to the phylogenetic pattern across elevational gradient in the Tibetan Plateau. This highlights the importance of considering not only abiotic filtering but also biotic interactions in soil bacterial communities across stressful elevational gradients.     

Coexistence between native and exotic species is facilitated by asymmetries in competitive ability and susceptibility to herbivores

Differences between native and exotic species in competitive ability and susceptibility to herbivores are hypothesized to facilitate coexistence. However, little fieldwork has been conducted to determine whether these differences are present in invaded communities. Here, we experimentally examined whether asymmetries exist between native and exotic plants in a community invaded for over 200 years and whether removing competitors or herbivores influences coexistence. We found that natives and exotics exhibit pronounced asymmetries, as exotics are competitively superior to natives, but are more significantly impacted by herbivores. We also found that herbivore removal mediated the outcome of competitive interactions and altered patterns of dominance across our field sites. Collectively, these findings suggest that asymmetric biotic interactions between native and exotic plants can help to facilitate coexistence in invaded communities.