Implications of Soil Microbial Community Assembly for Ecosystem Restoration: Patterns, Process, and Potential.

While it is now widely accepted that microorganisms provide essential functions in restoration ecology, the nature of relationships between microbial community assembly and ecosystem recovery remains unclear. There has been a longstanding challenge to decipher whether microorganisms facilitate or simply follow ecosystem recovery, and evidence for each is mixed at best. We propose that understanding microbial community assembly processes is critical to understanding the role of microorganisms during ecosystem restoration and thus optimizing management strategies. We examine how the connection between environment, community structure, and function is fundamentally underpinned by the processes governing community assembly of these microbial communities. We review important factors to consider in evaluating microbial community structure in the context of ecosystem recovery as revealed in studies of microbial succession: (1) variation in community assembly processes, (2) linkages to ecosystem function, and (3) measurable microbial community attributes. We seek to empower restoration ecology with microbial assembly and successional understandings that can generate actionable insights and vital contexts for ecosystem restoration efforts.

Plant community and soil chemistry responses to long-term nitrogen inputs drive changes in alpine bacterial communities.

Bacterial community composition and diversity was studied in alpine tundra soils across a plant species and moisture gradient in 20 y-old experimental plots with four nutrient addition regimes (control, nitrogen (N), phosphorus (P) or both nutrients). Different bacterial communities inhabited different alpine meadows, reflecting differences in moisture, nutrients and plant species. Bacterial community alpha-diversity metrics were strongly correlated with plant richness and the production of forbs. After meadow type, N addition proved the strongest determinant of bacterial community structure. Structural Equation Modeling demonstrated that tundra bacterial community responses to N addition occur via changes in plant community composition and soil pH resulting from N inputs, thus disentangling the influence of direct (resource availability) vs. indirect (changes in plant community structure and soil pH) N effects that have remained unexplored in past work examining bacterial responses to long-term N inputs in these vulnerable environments. Across meadow types, the relative influence of these indirect N effects on bacterial community structure varied. In explicitly evaluating the relative importance of direct and indirect effects of long-term N addition on bacterial communities, this study provides new mechanistic understandings of the interaction between plant and microbial community responses to N inputs amidst environmental change.

Interspecific Plant Interactions Reflected in Soil Bacterial Community Structure and Nitrogen Cycling in Primary Succession.

Past research demonstrating the importance plant-microbe interactions as drivers of ecosystem succession has focused on how plants condition soil microbial communities, impacting subsequent plant performance and plant community assembly. These studies, however, largely treat microbial communities as a black box. In this study, we sought to examine how emblematic shifts from early successional Alnus viridus ssp. sinuata (Sitka alder) to late successional Picea sitchensis (Sitka spruce) in primary succession may be reflected in specific belowground changes in bacterial community structure and nitrogen cycling related to the interaction of these two plants. We examined early successional alder-conditioned soils in a glacial forefield to delineate how alders alter the soil microbial community with increasing dominance. Further, we assessed the impact of late-successional spruce plants on these early successional alder-conditioned microbiomes and related nitrogen cycling through a leachate addition microcosm experiment. We show how increasingly abundant alder select for particular bacterial taxa. Additionally, we found that spruce leachate significantly alters the composition of these microbial communities in large part by driving declines in taxa that are enriched by alder, including bacterial symbionts. We found these effects to be spruce specific, beyond a general leachate effect. Our work also demonstrates a unique influence of spruce on ammonium availability. Such insights bolster theory relating the importance of plant-microbe interactions with late-successional plants and interspecific plant interactions more generally.

Oligotrophic wetland sediments susceptible to shifts in microbiomes and mercury cycling with dissolved organic matter addition.

Recent advances have allowed for greater investigation into microbial regulation of mercury toxicity in the environment. In wetlands in particular, dissolved organic matter (DOM) may influence methylmercury (MeHg) production both through chemical interactions and through substrate effects on microbiomes. We conducted microcosm experiments in two disparate wetland environments (oligotrophic unvegetated and high-C vegetated sediments) to examine the impacts of plant leachate and inorganic mercury loadings (20 mg/L HgCl2) on microbiomes and MeHg production in the St. Louis River Estuary. Our research reveals the greater relative capacity for mercury methylation in vegetated over unvegetated sediments. Further, our work shows how mercury cycling in oligotrophic unvegetated sediments may be susceptible to DOM inputs in the St. Louis River Estuary: unvegetated microcosms receiving leachate produced substantially more MeHg than unamended microcosms. We also demonstrate (1) changes in microbiome structure towards Clostridia, (2) metagenomic shifts toward fermentation, and (3) degradation of complex DOM; all of which coincide with elevated net MeHg production in unvegetated microcosms receiving leachate. Together, our work shows the influence of wetland vegetation in controlling MeHg production in the Great Lakes region and provides evidence that this may be due to both enhanced microbial activity as well as differences in microbiome composition.

Decreases in average bacterial community rRNA operon copy number during succession.

Trait-based studies can help clarify the mechanisms driving patterns of microbial community assembly and coexistence. Here, we use a trait-based approach to explore the importance of rRNA operon copy number in microbial succession, building on prior evidence that organisms with higher copy numbers respond more rapidly to nutrient inputs. We set flasks of heterotrophic media into the environment and examined bacterial community assembly at seven time points. Communities were arrayed along a geographic gradient to introduce stochasticity via dispersal processes and were analyzed using 16 S rRNA gene pyrosequencing, and rRNA operon copy number was modeled using ancestral trait reconstruction. We found that taxonomic composition was similar between communities at the beginning of the experiment and then diverged through time; as well, phylogenetic clustering within communities decreased over time. The average rRNA operon copy number decreased over the experiment, and variance in rRNA operon copy number was lowest both early and late in succession. We then analyzed bacterial community data from other soil and sediment primary and secondary successional sequences from three markedly different ecosystem types. Our results demonstrate that decreases in average copy number are a consistent feature of communities across various drivers of ecological succession. Importantly, our work supports the scaling of the copy number trait over multiple levels of biological organization, ranging from cells to populations and communities, with implications for both microbial ecology and evolution.

Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes?

Microorganisms are vital in mediating the earth's biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between microbial community structure and ecosystem processes remains poorly understood. Here, we address a fundamental and unanswered question in microbial ecology: 'When do we need to understand microbial community structure to accurately predict function?' We present a statistical analysis investigating the value of environmental data and microbial community structure independently and in combination for explaining rates of carbon and nitrogen cycling processes within 82 global datasets. Environmental variables were the strongest predictors of process rates but left 44% of variation unexplained on average, suggesting the potential for microbial data to increase model accuracy. Although only 29% of our datasets were significantly improved by adding information on microbial community structure, we observed improvement in models of processes mediated by narrow phylogenetic guilds via functional gene data, and conversely, improvement in models of facultative microbial processes via community diversity metrics. Our results also suggest that microbial diversity can strengthen predictions of respiration rates beyond microbial biomass parameters, as 53% of models were improved by incorporating both sets of predictors compared to 35% by microbial biomass alone. Our analysis represents the first comprehensive analysis of research examining links between microbial community structure and ecosystem function. Taken together, our results indicate that a greater understanding of microbial communities informed by ecological principles may enhance our ability to predict ecosystem process rates relative to assessments based on environmental variables and microbial physiology.

Nutrient addition dramatically accelerates microbial community succession.

The ecological mechanisms driving community succession are widely debated, particularly for microorganisms. While successional soil microbial communities are known to undergo predictable changes in structure concomitant with shifts in a variety of edaphic properties, the causal mechanisms underlying these patterns are poorly understood. Thus, to specifically isolate how nutrients--important drivers of plant succession--affect soil microbial succession, we established a full factorial nitrogen (N) and phosphorus (P) fertilization plot experiment in recently deglaciated (∼3 years since exposure), unvegetated soils of the Puca Glacier forefield in Southeastern Peru. We evaluated soil properties and examined bacterial community composition in plots before and one year after fertilization. Fertilized soils were then compared to samples from three reference successional transects representing advancing stages of soil development ranging from 5 years to 85 years since exposure. We found that a single application of +NP fertilizer caused the soil bacterial community structure of the three-year old soils to most resemble the 85-year old soils after one year. Despite differences in a variety of soil edaphic properties between fertilizer plots and late successional soils, bacterial community composition of +NP plots converged with late successional communities. Thus, our work suggests a mechanism for microbial succession whereby changes in resource availability drive shifts in community composition, supporting a role for nutrient colimitation in primary succession. These results suggest that nutrients alone, independent of other edaphic factors that change with succession, act as an important control over soil microbial community development, greatly accelerating the rate of succession.

Soil bacterial community structure remains stable over a 5-year chronosequence of insect-induced tree mortality.

Extensive tree mortality from insect epidemics has raised concern over possible effects on soil biogeochemical processes. Yet despite the importance of microbes in nutrient cycling, how soil bacterial communities respond to insect-induced tree mortality is largely unknown. We examined soil bacterial community structure (via 16S rRNA gene pyrosequencing) and community assembly processes (via null deviation analysis) along a 5-year chronosequence (substituting space for time) of bark beetle-induced tree mortality in the southern Rocky Mountains, USA. We also measured microbial biomass and soil chemistry, and used in situ experiments to assess inorganic nitrogen mineralization rates. We found that bacterial community structure and assembly-which was strongly influenced by stochastic processes-were largely unaffected by tree mortality despite increased soil ammonium ([Formula: see text]) pools and reductions in soil nitrate ([Formula: see text]) pools and net nitrogen mineralization rates after tree mortality. Linear models suggested that microbial biomass and bacterial phylogenetic diversity are significantly correlated with nitrogen mineralization rates of this forested ecosystem. However, given the overall resistance of the bacterial community to disturbance from tree mortality, soil nitrogen processes likely remained relatively stable following tree mortality when considered at larger spatial and longer temporal scales-a supposition supported by the majority of available studies regarding biogeochemical effects of bark beetle infestations in this region. Our results suggest that soil bacterial community resistance to disturbance helps to explain the relatively weak effects of insect-induced tree mortality on soil N and C pools reported across the Rocky Mountains, USA.

Patterns and processes of microbial community assembly.

Recent research has expanded our understanding of microbial community assembly. However, the field of community ecology is inaccessible to many microbial ecologists because of inconsistent and often confusing terminology as well as unnecessarily polarizing debates. Thus, we review recent literature on microbial community assembly, using the framework of Vellend (Q. Rev. Biol. 85:183-206, 2010) in an effort to synthesize and unify these contributions. We begin by discussing patterns in microbial biogeography and then describe four basic processes (diversification, dispersal, selection, and drift) that contribute to community assembly. We also discuss different combinations of these processes and where and when they may be most important for shaping microbial communities. The spatial and temporal scales of microbial community assembly are also discussed in relation to assembly processes. Throughout this review paper, we highlight differences between microbes and macroorganisms and generate hypotheses describing how these differences may be important for community assembly. We end by discussing the implications of microbial assembly processes for ecosystem function and biodiversity.

Changes in assembly processes in soil bacterial communities following a wildfire disturbance.

Although recent work has shown that both deterministic and stochastic processes are important in structuring microbial communities, the factors that affect the relative contributions of niche and neutral processes are poorly understood. The macrobiological literature indicates that ecological disturbances can influence assembly processes. Thus, we sampled bacterial communities at 4 and 16 weeks following a wildfire and used null deviation analysis to examine the role that time since disturbance has in community assembly. Fire dramatically altered bacterial community structure and diversity as well as soil chemistry for both time-points. Community structure shifted between 4 and 16 weeks for both burned and unburned communities. Community assembly in burned sites 4 weeks after fire was significantly more stochastic than in unburned sites. After 16 weeks, however, burned communities were significantly less stochastic than unburned communities. Thus, we propose a three-phase model featuring shifts in the relative importance of niche and neutral processes as a function of time since disturbance. Because neutral processes are characterized by a decoupling between environmental parameters and community structure, we hypothesize that a better understanding of community assembly may be important in determining where and when detailed studies of community composition are valuable for predicting ecosystem function.