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      Stochastic Assembly Leads to Alternative Communities with Distinct Functions in a Bioreactor Microbial Community

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          ABSTRACT

          The processes and mechanisms of community assembly and its relationships to community functioning are central issues in ecology. Both deterministic and stochastic factors play important roles in shaping community composition and structure, but the connection between community assembly and ecosystem functioning remains elusive, especially in microbial communities. Here, we used microbial electrolysis cell reactors as a model system to examine the roles of stochastic assembly in determining microbial community structure and functions. Under identical environmental conditions with the same source community, ecological drift (i.e., initial stochastic colonization) and subsequent biotic interactions created dramatically different communities with little overlap among 14 identical reactors, indicating that stochastic assembly played dominant roles in determining microbial community structure. Neutral community modeling analysis revealed that deterministic factors also played significant roles in shaping microbial community structure in these reactors. Most importantly, the newly formed communities differed substantially in community functions (e.g., H 2 production), which showed strong linkages to community structure. This study is the first to demonstrate that stochastic assembly plays a dominant role in determining not only community structure but also ecosystem functions. Elucidating the links among community assembly, biodiversity, and ecosystem functioning is critical to understanding ecosystem functioning, biodiversity preservation, and ecosystem management.

          IMPORTANCE

          Microorganisms are the most diverse group of life known on earth. Although it is well documented that microbial natural biodiversity is extremely high, it is not clear why such high diversity is generated and maintained. Numerous studies have established the roles of niche-based deterministic factors (e.g., pH, temperature, and salt) in shaping microbial biodiversity, the importance of stochastic processes in generating microbial biodiversity is rarely appreciated. Moreover, while microorganisms mediate many ecosystem processes, the relationship between microbial diversity and ecosystem functioning remains largely elusive. Using a well-controlled laboratory system, this study provides empirical support for the dominant role of stochastic assembly in creating variations of microbial diversity and the first explicit evidence for the critical role of community assembly in influencing ecosystem functioning. The results presented in this study represent important contributions to the understanding of the mechanisms, especially stochastic processes, involved in shaping microbial biodiversity.

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          Most cited references42

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          The diversity and biogeography of soil bacterial communities.

          For centuries, biologists have studied patterns of plant and animal diversity at continental scales. Until recently, similar studies were impossible for microorganisms, arguably the most diverse and abundant group of organisms on Earth. Here, we present a continental-scale description of soil bacterial communities and the environmental factors influencing their biodiversity. We collected 98 soil samples from across North and South America and used a ribosomal DNA-fingerprinting method to compare bacterial community composition and diversity quantitatively across sites. Bacterial diversity was unrelated to site temperature, latitude, and other variables that typically predict plant and animal diversity, and community composition was largely independent of geographic distance. The diversity and richness of soil bacterial communities differed by ecosystem type, and these differences could largely be explained by soil pH (r(2) = 0.70 and r(2) = 0.58, respectively; P < 0.0001 in both cases). Bacterial diversity was highest in neutral soils and lower in acidic soils, with soils from the Peruvian Amazon the most acidic and least diverse in our study. Our results suggest that microbial biogeography is controlled primarily by edaphic variables and differs fundamentally from the biogeography of "macro" organisms.
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            Stochastic and deterministic assembly processes in subsurface microbial communities.

            A major goal of microbial community ecology is to understand the forces that structure community composition. Deterministic selection by specific environmental factors is sometimes important, but in other cases stochastic or ecologically neutral processes dominate. Lacking is a unified conceptual framework aiming to understand why deterministic processes dominate in some contexts but not others. Here we work toward such a framework. By testing predictions derived from general ecological theory we aim to uncover factors that govern the relative influences of deterministic and stochastic processes. We couple spatiotemporal data on subsurface microbial communities and environmental parameters with metrics and null models of within and between community phylogenetic composition. Testing for phylogenetic signal in organismal niches showed that more closely related taxa have more similar habitat associations. Community phylogenetic analyses further showed that ecologically similar taxa coexist to a greater degree than expected by chance. Environmental filtering thus deterministically governs subsurface microbial community composition. More importantly, the influence of deterministic environmental filtering relative to stochastic factors was maximized at both ends of an environmental variation gradient. A stronger role of stochastic factors was, however, supported through analyses of phylogenetic temporal turnover. Although phylogenetic turnover was on average faster than expected, most pairwise comparisons were not themselves significantly non-random. The relative influence of deterministic environmental filtering over community dynamics was elevated, however, in the most temporally and spatially variable environments. Our results point to general rules governing the relative influences of stochastic and deterministic processes across micro- and macro-organisms.
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              Stochastic community assembly causes higher biodiversity in more productive environments.

              Net primary productivity is a principal driver of biodiversity; large-scale regions with higher productivity generally have more species. This pattern emerges because beta-diversity (compositional variation across local sites) increases with productivity, but the mechanisms underlying this phenomenon are unknown. Using data from a long-term experiment in replicate ponds, I show that higher beta-diversity at higher productivity resulted from a stronger role for stochastic relative to deterministic assembly processes with increasing productivity. This shift in the relative importance of stochasticity was most consistent with the hypothesis of more intense priority effects leading to multiple stable equilibria at higher productivity. Thus, shifts in community assembly mechanisms across a productivity gradient may underlie one of the most prominent biodiversity gradients on the planet.
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                Author and article information

                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society of Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                5 March 2013
                Mar-Apr 2013
                : 4
                : 2
                : e00584-12
                Affiliations
                State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China [ a ];
                Department of Microbiology and Plant Biology, Institute for Environmental Genomics and University of Oklahoma, Norman, Oklahoma, USA [ b ];
                Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA [ c ];
                State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin, China [ d ]
                Author notes
                Address correspondence to Jizhong Zhou, jzhou@ 123456ou.edu , or Aijie Wang, waj0578@ 123456hit.edu.cn .

                Editor Jo Handelsman, Yale University

                Article
                mBio00584-12
                10.1128/mBio.00584-12
                3585448
                23462114
                5a996452-f4ae-45b0-b70b-0b5ed13ca65e
                Copyright © 2013 Zhou et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 11 December 2012
                : 14 January 2013
                Page count
                Pages: 8
                Categories
                Research Article
                Custom metadata
                March/April 2013

                Life sciences
                Life sciences

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