Patterns and Processes of Microbial Community Assembly
01 Sep 2013-Microbiology and Molecular Biology Reviews (American Society for Microbiology)-Vol. 77, Iss: 3, pp 342-356
TL;DR: This review paper highlights differences between microbes and macroorganisms and generate hypotheses describing how these differences may be important for community assembly, and discusses the implications of microbial assembly processes for ecosystem function and biodiversity.
Abstract: SUMMARY 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 oftenconfusingterminologyaswellasunnecessarilypolarizingdebates. Thus,wereviewrecentliteratureonmicrobialcommunityassembly, using the framework of Vellend (Q. Rev. Biol. 85:183‐206, 2010) in an effort to synthesize and unify these contributions. We begin by discussingpatternsinmicrobialbiogeographyandthendescribefour basic processes (diversification, dispersal, selection, and drift) that contributetocommunityassembly.Wealsodiscussdifferentcombinations 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 generatehypothesesdescribinghowthesedifferencesmaybeimportantforcommunityassembly.Weendbydiscussingtheimplications ofmicrobialassemblyprocessesforecosystemfunctionandbiodiversity.
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American Museum of Natural History1, University of Tartu2, University of Colombo3, Royal Netherlands Academy of Arts and Sciences4, University of Florida5, University of Palermo6, Goethe University Frankfurt7, Hobart Corporation8, Nakhon Phanom University9, University of Bamenda10, University of Gothenburg11, Naturalis12, Swedish University of Agricultural Sciences13, Royal Botanic Gardens14, Universiti Malaysia Sabah15, United States Department of Agriculture16, Forest Research Institute Malaysia17, Humboldt State University18, Chinese Academy of Sciences19, Landcare Research20, University of Western Australia21, Estonian University of Life Sciences22, University of Southern Queensland23, Botanic Garden Meise24, Manchester Metropolitan University25, James Cook University26
TL;DR: Diversity of most fungal groups peaked in tropical ecosystems, but ectomycorrhizal fungi and several fungal classes were most diverse in temperate or boreal ecosystems, and manyfungal groups exhibited distinct preferences for specific edaphic conditions (such as pH, calcium, or phosphorus).
Abstract: Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and biogeographic patterns remain poorly understood. Using DNA metabarcoding data from hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled from plant diversity. The plant-to-fungus richness ratio declines exponentially toward the poles. Climatic factors, followed by edaphic and spatial variables, constitute the best predictors of fungal richness and community composition at the global scale. Fungi show similar latitudinal diversity gradients to other organisms, with several notable exceptions. These findings advance our understanding of global fungal diversity patterns and permit integration of fungi into a general macroecological framework.
2,346 citations
TL;DR: This finding indicates that hosts can benefit from microbial competition when this competition dampens cooperative networks and increases stability, and indicates that stability is promoted by limiting positive feedbacks and weakening ecological interactions.
Abstract: The human gut harbors a large and complex community of beneficial microbes that remain stable over long periods. This stability is considered critical for good health but is poorly understood. Here we develop a body of ecological theory to help us understand microbiome stability. Although cooperating networks of microbes can be efficient, we find that they are often unstable. Counterintuitively, this finding indicates that hosts can benefit from microbial competition when this competition dampens cooperative networks and increases stability. More generally, stability is promoted by limiting positive feedbacks and weakening ecological interactions. We have analyzed host mechanisms for maintaining stability—including immune suppression, spatial structuring, and feeding of community members—and support our key predictions with recent data.
1,443 citations
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 "Patterns and Processes of Microbial..."
...coupled with drift and diversification (67, 109)....
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...of birth, death, and reproduction (34, 67, 108) (Fig....
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...community assembly (67, 72, 108), but it is not accounted for in this framework (37)....
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...butions, species-area relationships, and distance-decay relationships (67, 72, 120)....
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...However, the identification and measurement of functional traits important for microbial community assembly and ecosystem functioning are a great challenge (67)....
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TL;DR: The conceptual and evidence-based foundation provided in this essay is expected to serve as a roadmap for hypothesis-driven, experimentally validated research on holobionts and their hologenomes, thereby catalyzing the continued fusion of biology's subdisciplines.
Abstract: Groundbreaking research on the universality and diversity of microorganisms is now challenging the life sciences to upgrade fundamental theories that once seemed untouchable. To fully appreciate the change that the field is now undergoing, one has to place the epochs and foundational principles of Darwin, Mendel, and the modern synthesis in light of the current advances that are enabling a new vision for the central importance of microbiology. Animals and plants are no longer heralded as autonomous entities but rather as biomolecular networks composed of the host plus its associated microbes, i.e., "holobionts." As such, their collective genomes forge a "hologenome," and models of animal and plant biology that do not account for these intergenomic associations are incomplete. Here, we integrate these concepts into historical and contemporary visions of biology and summarize a predictive and refutable framework for their evaluation. Specifically, we present ten principles that clarify and append what these concepts are and are not, explain how they both support and extend existing theory in the life sciences, and discuss their potential ramifications for the multifaceted approaches of zoology and botany. We anticipate that the conceptual and evidence-based foundation provided in this essay will serve as a roadmap for hypothesis-driven, experimentally validated research on holobionts and their hologenomes, thereby catalyzing the continued fusion of biology's subdisciplines. At a time when symbiotic microbes are recognized as fundamental to all aspects of animal and plant biology, the holobiont and hologenome concepts afford a holistic view of biological complexity that is consistent with the generally reductionist approaches of biology.
817 citations
Cites background from "Patterns and Processes of Microbial..."
...If microbial community structure and dynamics are primarily stochastic, then community composition should not differ from expectations based on random community assembly models [142,143]....
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TL;DR: The concepts and mechanisms of microbial resilience against dietary, antibiotic or bacteriotherapy-induced perturbations and the implications for human health are discussed.
Abstract: The resilience of the microbiota can protect us from disease, but a resilient dysbiotic microbiota may also cause disease. This Opinion article discusses the concepts and mechanisms of microbial resilience against dietary, antibiotic or bacteriotherapy-induced perturbations and the implications these have for human health. The composition of the intestinal microbiota varies among individuals and throughout development, and is dependent on host and environmental factors. However, although the microbiota is constantly exposed to environmental challenges, its composition and function in an individual are stable against perturbations, as microbial communities are resilient and resistant to change. The maintenance of a beneficial microbiota requires a homeostatic equilibrium within microbial communities, and also between the microorganisms and the intestinal interface of the host. The resilience of the healthy microbiota protects us from dysbiosis-related diseases, such as inflammatory bowel disease (IBD) or metabolic disorder. By contrast, a resilient dysbiotic microbiota may cause disease. In this Opinion article, we propose that microbial resilience has a key role in health and disease. We will discuss the concepts and mechanisms of microbial resilience against dietary, antibiotic or bacteriotherapy-induced perturbations and the implications for human health.
601 citations
References
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TL;DR: An overview of the analysis pipeline and links to raw data and processed output from the runs with and without denoising are provided.
Abstract: Supplementary Figure 1 Overview of the analysis pipeline. Supplementary Table 1 Details of conventionally raised and conventionalized mouse samples. Supplementary Discussion Expanded discussion of QIIME analyses presented in the main text; Sequencing of 16S rRNA gene amplicons; QIIME analysis notes; Expanded Figure 1 legend; Links to raw data and processed output from the runs with and without denoising.
28,911 citations
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01 Jan 2004TL;DR: In this paper, the authors focus on the pressure humanity is placing on the natural world, and on the continued ability of ecosystems to deliver the services on which we all depend, and develop strategies to ameliorate its impact.
Abstract: Summary As prehistoric cave paintings illustrate, our species has had an enduring appreciation of the variety and abundance of life on Earth. Today, however, concern is focused on the pressure humanity is placing on the natural world, and on the continued ability of ecosystems to deliver the services on which we all depend. To understand the extent of this ‘biodiversity crisis’ and develop strategies to ameliorate its impact, it is essential to be able to accurately measure biological diversity (a term often contracted to biodiversity) and make informed predictions about how and why this diversity varies over space and time.
7,082 citations
TL;DR: The results illustrate that UniFrac provides a new way of characterizing microbial communities, using the wealth of environmental rRNA sequences, and allows quantitative insight into the factors that underlie the distribution of lineages among environments.
Abstract: We introduce here a new method for computing differences between microbial communities based on phylogenetic information. This method, UniFrac, measures the phylogenetic distance between sets of taxa in a phylogenetic tree as the fraction of the branch length of the tree that leads to descendants from either one environment or the other, but not both. UniFrac can be used to determine whether communities are significantly different, to compare many communities simultaneously using clustering and ordination techniques, and to measure the relative contributions of different factors, such as chemistry and geography, to similarities between samples. We demonstrate the utility of UniFrac by applying it to published 16S rRNA gene libraries from cultured isolates and environmental clones of bacteria in marine sediment, water, and ice. Our results reveal that (i) cultured isolates from ice, water, and sediment resemble each other and environmental clone sequences from sea ice, but not environmental clone sequences from sediment and water; (ii) the geographical location does not correlate strongly with bacterial community differences in ice and sediment from the Arctic and Antarctic; and (iii) bacterial communities differ between terrestrially impacted seawater (whether polar or temperate) and warm oligotrophic seawater, whereas those in individual seawater samples are not more similar to each other than to those in sediment or ice samples. These results illustrate that UniFrac provides a new way of characterizing microbial communities, using the wealth of environmental rRNA sequences, and allows quantitative insight into the factors that underlie the distribution of lineages among environments.
6,679 citations
"Patterns and Processes of Microbial..." refers background in this paper
...Weighted UniFrac values (a measure of phylogenetic distance between communities [51, 52]) close to 1 indicate very different communities, and values close to 0 indicate almost identical communities....
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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