Stochastic Community Assembly: Does It Matter in Microbial Ecology?

Understanding the mechanisms controlling community diversity, functions, succession, and biogeography is a central, but poorly understood, topic in ecology, particularly in microbial ecology. Although stochastic processes are believed to play nonnegligible roles in shaping community structure, their importance relative to deterministic processes is hotly debated. The importance of ecological stochasticity in shaping microbial community structure is far less appreciated. Some of the main reasons for such heavy debates are the difficulty in defining stochasticity and the diverse methods used for delineating stochasticity. Here, we provide a critical review and synthesis of data from the most recent studies on stochastic community assembly in microbial ecology. We then describe both stochastic and deterministic components embedded in various ecological processes, including selection, dispersal, diversification, and drift. We also describe different approaches for inferring stochasticity from observational diversity patterns and highlight experimental approaches for delineating ecological stochasticity in microbial communities. In addition, we highlight research challenges, gaps, and future directions for microbial community assembly research

Dynamics of Sediment Microbial Functional Capacity and Community Interaction Networks in an Urbanized Coastal Estuary

Coastal estuaries and bays are exposed to both natural and anthropogenic environmental changes, inflicting intensive stress on the microbial communities inhabiting these areas. However, it remains unclear how microbial community diversity and their eco-functions are affected by anthropogenic disturbances rather than natural environmental changes. Here, we explored sediment microbial functional genes dynamics and community interaction networks in Hangzhou Bay (HZB), one of the most severely polluted bays on China’s eastern coast. The results indicated key microbial functional gene categories, including N, P, S, and aromatic compound metabolism, and stress response, displayed significant spatial dynamics along environmental gradients. Sensitive feedbacks of key functional gene categories to N and P pollutants demonstrated potential impacts of human-induced seawater pollutants to microbial functional capacity. Seawater ammonia and dissolved inorganic nitrogen (DIN) was identified as primary drivers in selecting adaptive populations and varying community composition. Network analysis revealed distinct modules that were stimulated in inner or outer bay. Importantly, the network keystone species, which played a fundamental role in community interactions, were strongly affected by N-pollutants. Our results provide a systematic understanding of the microbial compositional and functional dynamics in an urbanized coastal estuary, and highlighted the impact of human activities on these communities

A general framework for quantitatively assessing ecological stochasticity.

Understanding the community assembly mechanisms controlling biodiversity patterns is a central issue in ecology. Although it is generally accepted that both deterministic and stochastic processes play important roles in community assembly, quantifying their relative importance is challenging. Here we propose a general mathematical framework to quantify ecological stochasticity under different situations in which deterministic factors drive the communities more similar or dissimilar than null expectation. An index, normalized stochasticity ratio (NST), was developed with 50% as the boundary point between more deterministic (<50%) and more stochastic (>50%) assembly. NST was tested with simulated communities by considering abiotic filtering, competition, environmental noise, and spatial scales. All tested approaches showed limited performance at large spatial scales or under very high environmental noise. However, in all of the other simulated scenarios, NST showed high accuracy (0.90 to 1.00) and precision (0.91 to 0.99), with averages of 0.37 higher accuracy (0.1 to 0.7) and 0.33 higher precision (0.0 to 1.8) than previous approaches. NST was also applied to estimate stochasticity in the succession of a groundwater microbial community in response to organic carbon (vegetable oil) injection. Our results showed that community assembly was shifted from more deterministic (NST = 21%) to more stochastic (NST = 70%) right after organic carbon input. As the vegetable oil was consumed, the community gradually returned to be more deterministic (NST = 27%). In addition, our results demonstrated that null model algorithms and community similarity metrics had strong effects on quantifying ecological stochasticity

Microbial community assembly differs across minerals in a rhizosphere microcosm.

Mineral-associated microbes drive many critical soil processes, including mineral weathering, soil aggregation and cycling of mineral-sorbed organic matter. To investigate the interactions between soil minerals and microbes in the rhizosphere, we incubated three types of minerals (ferrihydrite, kaolinite and quartz) and a native soil mineral fraction near roots of a common Californian annual grass, Avena barbata, growing in its resident soil. We followed microbial colonization of these minerals for up to 2.5 months - the plant's lifespan. Bacteria and fungi that colonized mineral surfaces during this experiment differed across mineral types and differed from those in the background soil, implying that microbial colonization was the result of processes in addition to passive movement with water to mineral surfaces. Null model analysis revealed that dispersal limitation was a dominant factor structuring mineral-associated microbial communities for all mineral types. Once bacteria arrived at a mineral surface, capacity for rapid growth appeared important, as ribosomal copy number was significantly correlated with relative enrichment on minerals. Glomeromycota (a phylum associated with arbuscular mycorrhizal fungi) appeared to preferentially associate with ferrihydrite surfaces. The mechanisms enabling the colonization of soil minerals may be foundational in shaping the overall soil microbiome composition and development of persistent organic matter in soils

Oral microbiota of periodontal health and disease and their changes after nonsurgical periodontal therapy

This study examined the microbial diversity and community assembly of oral microbiota in periodontal health and disease and after nonsurgical periodontal treatment. The V4 region of 16S rRNA gene from DNA of 238 saliva and subgingival samples of 21 healthy and 48 diseased subjects was amplified and sequenced. Among 1979 OTUs identified, 28 were overabundant in diseased plaque. Six of these taxa were also overabundant in diseased saliva. Twelve OTUs were overabundant in healthy plaque. There was a trend for disease-associated taxa to decrease and health-associated taxa to increase after treatment with notable variations among individual sites. Network analysis revealed modularity of the microbial communities and identified several health- and disease-specific modules. Ecological drift was a major factor that governed community turnovers in both plaque and saliva. Dispersal limitation and homogeneous selection affected the community assembly in plaque, with the additional contribution of homogenizing dispersal for plaque within individuals. Homogeneous selection and dispersal limitation played important roles, respectively, in healthy saliva and diseased pre-treatment saliva between individuals. Our results revealed distinctions in both taxa and assembly processes of oral microbiota between periodontal health and disease. Furthermore, the community assembly analysis has identified potentially effective approaches for managing periodontitis

Functional Gene Array-Based Ultrasensitive and Quantitative Detection of Microbial Populations in Complex Communities.

While functional gene arrays (FGAs) have greatly expanded our understanding of complex microbial systems, specificity, sensitivity, and quantitation challenges remain. We developed a new generation of FGA, GeoChip 5.0, using the Agilent platform. Two formats were created, a smaller format (GeoChip 5.0S), primarily covering carbon-, nitrogen-, sulfur-, and phosphorus-cycling genes and others providing ecological services, and a larger format (GeoChip 5.0M) containing the functional categories involved in biogeochemical cycling of C, N, S, and P and various metals, stress response, microbial defense, electron transport, plant growth promotion, virulence, gyrB, and fungus-, protozoan-, and virus-specific genes. GeoChip 5.0M contains 161,961 oligonucleotide probes covering >365,000 genes of 1,447 gene families from broad, functionally divergent taxonomic groups, including bacteria (2,721 genera), archaea (101 genera), fungi (297 genera), protists (219 genera), and viruses (167 genera), mainly phages. Computational and experimental evaluation indicated that designed probes were highly specific and could detect as little as 0.05 ng of pure culture DNAs within a background of 1 μg community DNA (equivalent to 0.005% of the population). Additionally, strong quantitative linear relationships were observed between signal intensity and amount of pure genomic (∼99% of probes detected; r > 0.9) or soil (∼97%; r > 0.9) DNAs. Application of the GeoChip to a contaminated groundwater microbial community indicated that environmental contaminants (primarily heavy metals) had significant impacts on the biodiversity of the communities. This is the most comprehensive FGA to date, capable of directly linking microbial genes/populations to ecosystem functions.IMPORTANCE The rapid development of metagenomic technologies, including microarrays, over the past decade has greatly expanded our understanding of complex microbial systems. However, because of the ever-expanding number of novel microbial sequences discovered each year, developing a microarray that is representative of real microbial communities, is specific and sensitive, and provides quantitative information remains a challenge. The newly developed GeoChip 5.0 is the most comprehensive microarray available to date for examining the functional capabilities of microbial communities important to biogeochemistry, ecology, environmental sciences, and human health. The GeoChip 5 is highly specific, sensitive, and quantitative based on both computational and experimental assays. Use of the array on a contaminated groundwater sample provided novel insights on the impacts of environmental contaminants on groundwater microbial communities

Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity.

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

Continental scale structuring of forest and soil diversity via functional traits.

Trait-based ecology claims to offer a mechanistic approach for explaining the drivers that structure biological diversity and predicting the responses of species, trophic interactions and ecosystems to environmental change. However, support for this claim is lacking across broad taxonomic groups. A framework for defining ecosystem processes in terms of the functional traits of their constituent taxa across large spatial scales is needed. Here, we provide a comprehensive assessment of the linkages between climate, plant traits and soil microbial traits at many sites spanning a broad latitudinal temperature gradient from tropical to subalpine forests. Our results show that temperature drives coordinated shifts in most plant and soil bacterial traits but these relationships are not observed for most fungal traits. Shifts in plant traits are mechanistically associated with soil bacterial functional traits related to carbon (C), nitrogen (N) and phosphorus (P) cycling, indicating that microbial processes are tightly linked to variation in plant traits that influence rates of ecosystem decomposition and nutrient cycling. Our results are consistent with hypotheses that diversity gradients reflect shifts in phenotypic optima signifying local temperature adaptation mediated by soil nutrient availability and metabolism. They underscore the importance of temperature in structuring the functional diversity of plants and soil microbes in forest ecosystems and how this is coupled to biogeochemical processes via functional traits

Nearly a decade-long repeatable seasonal diversity patterns of bacterioplankton communities in the eutrophic Lake Donghu (Wuhan, China).

Uncovering which environmental factors govern community diversity patterns and how ecological processes drive community turnover are key questions related to understand the community assembly. However, the ecological mechanisms regulating long-term variations of bacterioplankton communities in lake ecosystems remain poorly understood. Here we present nearly a decade-long study of bacterioplankton communities from the eutrophic Lake Donghu (Wuhan, China) using 16S rRNA gene amplicon sequencing with MiSeq platform. We found strong repeatable seasonal diversity patterns in terms of both common (detected in more than 50% samples) and dominant (relative abundance >1%) bacterial taxa turnover. Moreover, community composition tracked the seasonal temperature gradient, indicating that temperature is a key environmental factor controlling observed diversity patterns. Total phosphorus also contributed significantly to the seasonal shifts in bacterioplankton composition. However, any spatial pattern of bacterioplankton communities across the main lake areas within season was overwhelmed by their temporal variabilities. Phylogenetic analysis further indicated that 75%-82% of community turnover was governed by homogeneous selection due to consistent environmental conditions within seasons, suggesting that the microbial communities in Lake Donghu are mainly controlled by niche-based processes. Therefore, dominant niches available within seasons might be occupied by similar combinations of bacterial taxa with modest dispersal rates throughout different lake areas

Climate warming accelerates temporal scaling of grassland soil microbial biodiversity.

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 < 0.001) higher temporal scaling rates. While the STRs and PTRs were significantly shifted by altered precipitation, clipping and their combinations, warming played the predominant role. In addition, comparison with the previous literature revealed that soil bacteria and fungi had considerably higher overall temporal scaling rates (w = 0.39-0.64) than those of plants and animals (w = 0.21-0.38). Our results on warming-enhanced temporal scaling of microbial biodiversity suggest that the strategies of soil biodiversity preservation and ecosystem management may need to be adjusted in a warmer world