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      Strong inter-population cooperation leads to partner intermixing in microbial communities

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          Abstract

          Patterns of spatial positioning of individuals within microbial communities are often critical to community function. However, understanding patterning in natural communities is hampered by the multitude of cell–cell and cell–environment interactions as well as environmental variability. Here, through simulations and experiments on communities in defined environments, we examined how ecological interactions between two distinct partners impacted community patterning. We found that in strong cooperation with spatially localized large fitness benefits to both partners, a unique pattern is generated: partners spatially intermixed by appearing successively on top of each other, insensitive to initial conditions and interaction dynamics. Intermixing was experimentally observed in two obligatory cooperative systems: an engineered yeast community cooperating through metabolite-exchanges and a methane-producing community cooperating through redox-coupling. Even in simulated communities consisting of several species, most of the strongly-cooperating pairs appeared intermixed. Thus, when ecological interactions are the major patterning force, strong cooperation leads to partner intermixing.

          DOI: http://dx.doi.org/10.7554/eLife.00230.001

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          Microorganisms such as bacteria, archaea and tiny eukaryotes are found throughout the biosphere. Some of these microorganisms are pathogens that cause diseases in animals, while others provide nutrients, including essential amino acids and vitamins; there are also microorganisms that have critical roles in recycling elements such as carbon, nitrogen and oxygen in the biosphere. In the natural world, microorganisms interact with their environment and with each other, often competing for space, light and nutrients, but sometimes they act cooperatively, which benefits all parties involved.

          Microbial communities exhibit spatial patterns that reflect the relative positioning of different microbes in a community. These patterns can be critical for the proper functioning of a microbial community. For example, in the microbial granules that digest organic compounds in waste water, the stratified pattern of different microbial species can be thought of as a sequence of catalysts needed to perform a series of biochemical processing steps. Thus, it is important to understand the mechanisms that drive pattern formation in multispecies communities.

          Now, through a combination of simulations and experiments, Momeni et al. have identified two features of spatial patterns in two-population microbial communities when pattern formation is driven by fitness effects related to the ecological interactions between cells. First, interactions that confer significant advantages to at least one of the populations can potentially result in the generation of a stable community; the community is stable in the sense that if it is disturbed, it will return to its stable population composition following the disturbance. Indeed, in engineered Saccharomyces cerevisiae communities, very different initial population ratios converged to the same value over time when one strain depended on the other strain, or when the two strains depended on each other, but not when the two strains competed.

          The second feature applies to microbial communities composed of two cooperating populations: whereas two populations that compete with each other tend to segregate, cooperation results in the members of the two populations mixing together. Momeni et al. observe the formation of such an “intermixed” community in simulations, and also in two experimental systems that involve cooperation—a community containing two different strains of yeast cooperating through metabolite exchange, and a biofilm in which Methanococcus maripaludis, an archaeon that produces methane, cooperates with the bacterium Desulfovibrio vulgaris.

          These two features of spatial patterning are conceptually similar to the competitive exclusion principle, which states that two species competing for the same resources cannot stably coexist if competition is the sole force at work. This principle has, therefore, encouraged scientists to search for the other forces that must be responsible for the coexistence of different species. Similarly, by predicting the sorts of patterns that will form when the fitness effects of ecological interactions between cells are the only forces at work, Momeni et al. lay the groundwork for investigations into other mechanisms, such as cell–environment interactions and active cell motility, that can govern pattern formation in microbial communities.

          DOI: http://dx.doi.org/10.7554/eLife.00230.002

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          Most cited references45

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          Oral multispecies biofilm development and the key role of cell-cell distance.

          Growth of oral bacteria in situ requires adhesion to a surface because the constant flow of host secretions thwarts the ability of planktonic cells to grow before they are swallowed. Therefore, oral bacteria evolved to form biofilms on hard tooth surfaces and on soft epithelial tissues, which often contain multiple bacterial species. Because these biofilms are easy to study, they have become the paradigm of multispecies biofilms. In this Review we describe the factors involved in the formation of these biofilms, including the initial adherence to the oral tissues and teeth, cooperation between bacterial species in the biofilm, signalling between the bacteria and its role in pathogenesis, and the transfer of DNA between bacteria. In all these aspects distance between cells of different species is integral for oral biofilm growth.
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            Sociomicrobiology: the connections between quorum sensing and biofilms.

            In the past decade, significant debate has surrounded the relative contributions of genetic determinants versus environmental conditions to certain types of human behavior. While this debate goes on, it is with a certain degree of irony that microbiologists studying aspects of bacterial community behavior face the same questions. Information regarding two social phenomena exhibited by bacteria, quorum sensing and biofilm development, is reviewed here. These two topics have been inextricably linked, possibly because biofilms and quorum sensing represent two areas in which microbiologists focus on social aspects of bacteria. We will examine what is known about this linkage and discuss areas that might be developed. In addition, we believe that these two aspects of bacterial behavior represent a small part of the social repertoire of bacteria. Bacteria exhibit many social activities and they represent a model for dissecting social behavior at the genetic level. Therefore, we introduce the term 'sociomicrobiology'.
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              Getting started with yeast.

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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                2050-084X
                22 January 2013
                2013
                : 2
                : e00230
                Affiliations
                [1]deptDivision of Basic Sciences , Fred Hutchinson Cancer Research Center , Seattle, United States
                [2]deptDepartment of Microbiology and Center for Biofilm Engineering , Montana State University , Bozeman, United States
                Max Planck Institute for Evolutionary Biology , Germany
                Author notes
                [* ]For correspondence: bmomeni@ 123456fhcrc.org (BM);
                [* ]For correspondence: wenying.shou@ 123456gmail.com (WS)
                Article
                00230
                10.7554/eLife.00230
                3552619
                23359860
                678043ee-ab12-4461-b9bb-192956b79d2f
                © 2013, Momeni et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 10 September 2012
                : 27 November 2012
                Funding
                Funded by: Gordon and Betty Moore Foundation;
                Award Recipient :
                Funded by: Life Science Research Foundation;
                Award Recipient :
                Funded by: National Science Foundation;
                Award Recipient :
                Funded by: United States Department of Energy;
                Award ID: DE-AC02-05CH11231
                Award Recipient :
                Funded by: National Institutes of Health;
                Award ID: DP2 OD006498-01
                Award Recipient :
                Funded by: W. M. Keck Foundation;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Biophysics and Structural Biology
                Microbiology and Infectious Disease
                Custom metadata
                2
                Simulations and experiments on systems containing two different populations of microorganisms show that interactions that benefit at least one of the populations can lead to communities with stable compositions, and that strong cooperation between two populations can lead to communities in which both populations are mixed together.

                Life sciences
                pattern formation,microbial communities,cooperation,ecological interactions,methanogenic biofilms,syntrophic biofilms,s. cerevisiae

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