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Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community.

Zhou J, Liu W, Deng Y, Jiang YH, Xue K, He Z, Van Nostrand JD, Wu L, Yang Y, Wang A - MBio (2013)

Bottom Line: Neutral community modeling analysis revealed that deterministic factors also played significant roles in shaping microbial community structure in these reactors.Moreover, while microorganisms mediate many ecosystem processes, the relationship between microbial diversity and ecosystem functioning remains largely elusive.The results presented in this study represent important contributions to the understanding of the mechanisms, especially stochastic processes, involved in shaping microbial biodiversity.

View Article: PubMed Central - PubMed

Affiliation: State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China. jzhou@ou.edu

ABSTRACT
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., H2 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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Stochastic community assembly processes in the MECs. The diagram shows a schematic of neutral dynamics in the assembly of the MEC reactor biofilm community. It is assumed that the regional pool has 20 individuals of 5 species (A, B, C, D, and E), with each species having a different abundance (A). During the initial inoculation, different species colonize the anodes of the MECs to produce current. Due to the stochastic process of colonization, the established biofilm composition varies considerably among different MEC reactors to form 4 different community structure states (B). Following that, the reactor solutions were replaced with new sterile medium every 24 h. Due to competition for resources and space, some species could detach from the biofilm and subsequently be lost during medium exchange, whereas some species could recolonize the anodes, which further creates variation of the communities among different bioreactors (C). Thus, even though these reactors were operated under identical conditions with the same source community, the community structures were quite different due to ecological drift in colonization.
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fig1: Stochastic community assembly processes in the MECs. The diagram shows a schematic of neutral dynamics in the assembly of the MEC reactor biofilm community. It is assumed that the regional pool has 20 individuals of 5 species (A, B, C, D, and E), with each species having a different abundance (A). During the initial inoculation, different species colonize the anodes of the MECs to produce current. Due to the stochastic process of colonization, the established biofilm composition varies considerably among different MEC reactors to form 4 different community structure states (B). Following that, the reactor solutions were replaced with new sterile medium every 24 h. Due to competition for resources and space, some species could detach from the biofilm and subsequently be lost during medium exchange, whereas some species could recolonize the anodes, which further creates variation of the communities among different bioreactors (C). Thus, even though these reactors were operated under identical conditions with the same source community, the community structures were quite different due to ecological drift in colonization.

Mentions: The establishment and dynamics of the biofilm communities in MEC reactors are ideal for examining the role of stochastic processes (i.e., colonization and extinction) in community assembly (34) (Fig. 1). Many replicate reactors can be set up with the same wastewater inoculum and operated under identical environmental conditions. The wastewater inoculum generally contains many different microbial populations (Fig. 1A) that can potentially colonize the anode by random chance. Due to such stochastic colonization, considerable site-to-site variation (unpredictability) in community composition could exist under identical environmental conditions (Fig. 1B). Such unpredictability could also be intensified by subsequent deterministic processes through species selection, priority effects, and population interactions (Fig. 1C). After initial colonization, some species could come off anode biofilm and be lost during medium exchanges, which is a proxy for the species extinction process. Thus, the final community structure could be dependent on stochastic ecological drift (i.e., initial stochastic colonization and subsequent extinction) as well as priority effects and species interactions.


Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community.

Zhou J, Liu W, Deng Y, Jiang YH, Xue K, He Z, Van Nostrand JD, Wu L, Yang Y, Wang A - MBio (2013)

Stochastic community assembly processes in the MECs. The diagram shows a schematic of neutral dynamics in the assembly of the MEC reactor biofilm community. It is assumed that the regional pool has 20 individuals of 5 species (A, B, C, D, and E), with each species having a different abundance (A). During the initial inoculation, different species colonize the anodes of the MECs to produce current. Due to the stochastic process of colonization, the established biofilm composition varies considerably among different MEC reactors to form 4 different community structure states (B). Following that, the reactor solutions were replaced with new sterile medium every 24 h. Due to competition for resources and space, some species could detach from the biofilm and subsequently be lost during medium exchange, whereas some species could recolonize the anodes, which further creates variation of the communities among different bioreactors (C). Thus, even though these reactors were operated under identical conditions with the same source community, the community structures were quite different due to ecological drift in colonization.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3585448&req=5

fig1: Stochastic community assembly processes in the MECs. The diagram shows a schematic of neutral dynamics in the assembly of the MEC reactor biofilm community. It is assumed that the regional pool has 20 individuals of 5 species (A, B, C, D, and E), with each species having a different abundance (A). During the initial inoculation, different species colonize the anodes of the MECs to produce current. Due to the stochastic process of colonization, the established biofilm composition varies considerably among different MEC reactors to form 4 different community structure states (B). Following that, the reactor solutions were replaced with new sterile medium every 24 h. Due to competition for resources and space, some species could detach from the biofilm and subsequently be lost during medium exchange, whereas some species could recolonize the anodes, which further creates variation of the communities among different bioreactors (C). Thus, even though these reactors were operated under identical conditions with the same source community, the community structures were quite different due to ecological drift in colonization.
Mentions: The establishment and dynamics of the biofilm communities in MEC reactors are ideal for examining the role of stochastic processes (i.e., colonization and extinction) in community assembly (34) (Fig. 1). Many replicate reactors can be set up with the same wastewater inoculum and operated under identical environmental conditions. The wastewater inoculum generally contains many different microbial populations (Fig. 1A) that can potentially colonize the anode by random chance. Due to such stochastic colonization, considerable site-to-site variation (unpredictability) in community composition could exist under identical environmental conditions (Fig. 1B). Such unpredictability could also be intensified by subsequent deterministic processes through species selection, priority effects, and population interactions (Fig. 1C). After initial colonization, some species could come off anode biofilm and be lost during medium exchanges, which is a proxy for the species extinction process. Thus, the final community structure could be dependent on stochastic ecological drift (i.e., initial stochastic colonization and subsequent extinction) as well as priority effects and species interactions.

Bottom Line: Neutral community modeling analysis revealed that deterministic factors also played significant roles in shaping microbial community structure in these reactors.Moreover, while microorganisms mediate many ecosystem processes, the relationship between microbial diversity and ecosystem functioning remains largely elusive.The results presented in this study represent important contributions to the understanding of the mechanisms, especially stochastic processes, involved in shaping microbial biodiversity.

View Article: PubMed Central - PubMed

Affiliation: State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China. jzhou@ou.edu

ABSTRACT
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., H2 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.

Show MeSH
Related in: MedlinePlus