Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community.
TL;DR: This study is the first to demonstrate that stochastic assembly plays a dominant role in determining not only community structure but also ecosystem functions, and the first explicit evidence for the critical role of community assembly in influencing ecosystem functioning.
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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TL;DR: Both stochastic and deterministic components embedded in various ecological processes, including selection, dispersal, diversification, and drift are described.
Abstract: 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.
1,071 citations
Cites background from "Stochastic assembly leads to altern..."
...history affects ecosystem functioning (36, 253)....
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..., initial stochastic colonization) and subsequent biotic interactions via priority effects were critical in determining microbial community structure (36)....
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...although deterministic processes were also important (32, 36, 177, 178, 193)....
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...nogenesis, or CO2 production via fermentation) (36)....
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...Although various experimental studies revealed that historical contingency affects community structure, little is known about whether historical contingency affects community functioning (36, 253)....
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TL;DR: This study shows that the succession of groundwater microbial communities in response to nutrient amendment is primarily stochastic, but that the drivers controlling biodiversity and succession are dynamic rather than static, and identifies the mechanisms controlling microbial community assembly and succession.
Abstract: Unraveling the drivers of community structure and succession in response to environmental change is a central goal in ecology. Although the mechanisms shaping community structure have been intensively examined, those controlling ecological succession remain elusive. To understand the relative importance of stochastic and deterministic processes in mediating microbial community succession, a unique framework composed of four different cases was developed for fluidic and nonfluidic ecosystems. The framework was then tested for one fluidic ecosystem: a groundwater system perturbed by adding emulsified vegetable oil (EVO) for uranium immobilization. Our results revealed that groundwater microbial community diverged substantially away from the initial community after EVO amendment and eventually converged to a new community state, which was closely clustered with its initial state. However, their composition and structure were significantly different from each other. Null model analysis indicated that both deterministic and stochastic processes played important roles in controlling the assembly and succession of the groundwater microbial community, but their relative importance was time dependent. Additionally, consistent with the proposed conceptual framework but contradictory to conventional wisdom, the community succession responding to EVO amendment was primarily controlled by stochastic rather than deterministic processes. During the middle phase of the succession, the roles of stochastic processes in controlling community composition increased substantially, ranging from 81.3% to 92.0%. Finally, there are limited successional studies available to support different cases in the conceptual framework, but further well-replicated explicit time-series experiments are needed to understand the relative importance of deterministic and stochastic processes in controlling community succession.
525 citations
Cites background from "Stochastic assembly leads to altern..."
...Proc Natl Acad Sci USA 108(14):5643–5648....
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...When stochastic processes are coupled with priority effects, where early-arriving species influence the establishment and growth of later-arriving species (12), local communities with greater site-to-site variations (high β-diversity) in species compositions can emerge under similar, even identical, environmental conditions (10, 13, 14)....
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Tsinghua University1, Southwest University2, University of Oklahoma3, Newcastle University4, Northeastern University (China)5, Washington University in St. Louis6, University of Vienna7, Northwestern University8, Chinese Academy of Sciences9, Shandong University10, University of Hong Kong11, Sun Yat-sen University12, University of Queensland13, Aalborg University14, Rice University15, Stanford University16, Michigan State University17, University of Tennessee18, University of Washington19, Lawrence Berkeley National Laboratory20, Arizona State University21
TL;DR: Global sampling of microbial communities associated with wastewater treatment plants and application of ecological theory revealed a small, core bacterial community associated with performance and provides insights into the community dynamics in this environment.
Abstract: Microorganisms in wastewater treatment plants (WWTPs) are essential for water purification to protect public and environmental health. However, the diversity of microorganisms and the factors that control it are poorly understood. Using a systematic global-sampling effort, we analysed the 16S ribosomal RNA gene sequences from ~1,200 activated sludge samples taken from 269 WWTPs in 23 countries on 6 continents. Our analyses revealed that the global activated sludge bacterial communities contain ~1 billion bacterial phylotypes with a Poisson lognormal diversity distribution. Despite this high diversity, activated sludge has a small, global core bacterial community (n = 28 operational taxonomic units) that is strongly linked to activated sludge performance. Meta-analyses with global datasets associate the activated sludge microbiomes most closely to freshwater populations. In contrast to macroorganism diversity, activated sludge bacterial communities show no latitudinal gradient. Furthermore, their spatial turnover is scale-dependent and appears to be largely driven by stochastic processes (dispersal and drift), although deterministic factors (temperature and organic input) are also important. Our findings enhance our mechanistic understanding of the global diversity and biogeography of activated sludge bacterial communities within a theoretical ecology framework and have important implications for microbial ecology and wastewater treatment processes.
423 citations
TL;DR: This is the first study demonstrating that the diversity of different microbial groups has significantly lower rates of turnover across temperature gradients than other major taxa, which has important implications for assessing the effects of human-caused changes in climate, land use and other factors.
Abstract: Climate warming is increasingly leading to marked changes in plant and animal biodiversity, but it remains unclear how temperatures affect microbial biodiversity, particularly in terrestrial soils. Here we show that, in accordance with metabolic theory of ecology, taxonomic and phylogenetic diversity of soil bacteria, fungi and nitrogen fixers are all better predicted by variation in environmental temperature than pH. However, the rates of diversity turnover across the global temperature gradients are substantially lower than those recorded for trees and animals, suggesting that the diversity of plant, animal and soil microbial communities show differential responses to climate change. To the best of our knowledge, this is the first study demonstrating that the diversity of different microbial groups has significantly lower rates of turnover across temperature gradients than other major taxa, which has important implications for assessing the effects of human-caused changes in climate, land use and other factors.
383 citations
TL;DR: 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 is proposed.
Abstract: 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%) 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.
370 citations
Cites background from "Stochastic assembly leads to altern..."
...However, most null model-based inferences on community assembly mechanisms are qualitative rather than quantitative (6, 7, 13, 19, 22, 25)....
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...However, determining their relative importance in governing community diversity, especially in microbial ecology, is still challenging (3, 5, 12, 13)....
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References
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01 Jan 2001TL;DR: A study of the issue indicates that it is not a serious problem for neutral theory, and there is sometimes a difference between some of the simulation-based results of Hubbell and the analytical results of Volkov et al. (2003).
Abstract: study of the issue indicates that it is not a serious problem for neutral theory, for reasons we discuss below. First, a bit of background. Hubbell (2001) derived the analytical expression for the stochastic mean and variance of the abundance of a single arbitrary species in a neutral community undergoing immigration from a metacommunity source area. However, his approach did not lend itself to an analytical solution for the distribution of relative species abundance (RSA) in a multispecies community for community sizes larger than a handful of individuals. As a result, all of Hubbell's RSA distributions for local communities were based on simulations. This problem was solved by Volkov et al. (2003), who derived an analytical expression for the RSA distribution in local communities of arbitrary size. However, as Chisholm and Burgman noted, there is sometimes a difference between some of the simulation-based results of Hubbell and the analytical results of Volkov et al. (2003). Chisholm and Burgman computed Volkov's equation and resimulated Hubbell's results for the four cases
5,317 citations
TL;DR: Stabilizing mechanisms are essential for species coexistence and include traditional mechanisms such as resource partitioning and frequency-dependent predation, as well as mechanisms that depend on fluctuations in population densities and environmental factors in space and time.
Abstract: ▪ Abstract The focus of most ideas on diversity maintenance is species coexistence, which may be stable or unstable. Stable coexistence can be quantified by the long-term rates at which community members recover from low density. Quantification shows that coexistence mechanisms function in two major ways: They may be (a) equalizing because they tend to minimize average fitness differences between species, or (b) stabilizing because they tend to increase negative intraspecific interactions relative to negative interspecific interactions. Stabilizing mechanisms are essential for species coexistence and include traditional mechanisms such as resource partitioning and frequency-dependent predation, as well as mechanisms that depend on fluctuations in population densities and environmental factors in space and time. Equalizing mechanisms contribute to stable coexistence because they reduce large average fitness inequalities which might negate the effects of stabilizing mechanisms. Models of unstable coexitence...
5,240 citations
"Stochastic assembly leads to altern..." refers background in this paper
..., competition, predation, mutualism), and environmental conditions, govern species diversity and composition of a local community (7, 8), and hence community composition should converge toward a single pattern under similar environmental conditions, while communities under different environmental conditions will have divergent configurations (5)....
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TL;DR: 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 this study.
Abstract: 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.
4,376 citations
TL;DR: Larger numbers of species are probably needed to reduce temporal variability in ecosystem processes in changing environments and to determine how biodiversity dynamics, ecosystem processes, and abiotic factors interact.
Abstract: The ecological consequences of biodiversity loss have aroused considerable interest and controversy during the past decade. Major advances have been made in describing the relationship between species diversity and ecosystem processes, in identifying functionally important species, and in revealing underlying mechanisms. There is, however, uncertainty as to how results obtained in recent experiments scale up to landscape and regional levels and generalize across ecosystem types and processes. Larger numbers of species are probably needed to reduce temporal variability in ecosystem processes in changing environments. A major future challenge is to determine how biodiversity dynamics, ecosystem processes, and abiotic factors interact.
4,070 citations
TL;DR: Four methods for purifying crude DNA were evaluated for percent recovery, fragment size, speed, enzyme restriction, PCR amplification, and DNA-DNA hybridization and in general, all methods produced DNA pure enough for PCR amplification.
Abstract: A simple, rapid method for bacterial lysis and direct extraction of DNA from soils with minimal shearing was developed to address the risk of chimera formation from small template DNA during subsequent PCR. The method was based on lysis with a high-salt extraction buffer (1.5 M NaCl) and extended heating (2 to 3 h) of the soil suspension in the presence of sodium dodecyl sulfate (SDS), hexadecyltrimethylammonium bromide, and proteinase K. The extraction method required 6 h and was tested on eight soils differing in organic carbon, clay content, and pH, including ones from which DNA extraction is difficult. The DNA fragment size in crude extracts from all soils was > 23 kb. Preliminary trials indicated that DNA recovery from two soils seeded with gram-negative bacteria was 92 to 99%. When the method was tested on all eight unseeded soils, microscopic examination of indigenous bacteria in soil pellets before and after extraction showed variable cell lysis efficiency (26 to 92%). Crude DNA yields from the eight soils ranged from 2.5 to 26.9 micrograms of DNA g-1, and these were positively correlated with the organic carbon content in the soil (r = 0.73). DNA yields from gram-positive bacteria from pure cultures were two to six times higher when the high-salt-SDS-heat method was combined with mortar-and-pestle grinding and freeze-thawing, and most DNA recovered was of high molecular weight. Four methods for purifying crude DNA were also evaluated for percent recovery, fragment size, speed, enzyme restriction, PCR amplification, and DNA-DNA hybridization. In general, all methods produced DNA pure enough for PCR amplification. Since soil type and microbial community characteristics will influence DNA recovery, this study provides guidance for choosing appropriate extraction and purification methods on the basis of experimental goals.
2,826 citations
"Stochastic assembly leads to altern..." refers methods in this paper
...Community DNA from representative samples was extracted using the mechanical grinding and SDS-based chemical lysis method (56)....
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