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Competition for space during bacterial colonization of a surface.

ABSTRACT: Competition for space is ubiquitous in the ecology of both microorganisms and macro-organisms. We introduce a bacterial model system in which the factors influencing competition for space during colonization of an initially empty habitat can be tracked directly. Using fluorescence microscopy, we follow the fate of individual Escherichia coli bacterial cell lineages as they undergo expansion competition (the race to be the first to colonize a previously empty territory), and as they later compete at boundaries between clonal territories. Our experiments are complemented by computer simulations of a lattice-based model. We find that both expansion competition, manifested as differences in individual cell lag times, and boundary competition, manifested as effects of neighbour cell geometry, can play a role in colonization success, particularly when lineages expand exponentially. This work provides a baseline for investigating how ecological interactions affect colonization of space by bacterial populations, and highlights the potential of bacterial model systems for the testing and development of ecological theory.

SUBMITTER: Lloyd DP

PROVIDER: S-EPMC4614474 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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Competition for space during bacterial colonization of a surface.

Lloyd Diarmuid P DP Allen Rosalind J RJ Allen Rosalind J RJ

Journal of the Royal Society, Interface 20150901 110

Competition for space is ubiquitous in the ecology of both microorganisms and macro-organisms. We introduce a bacterial model system in which the factors influencing competition for space during colonization of an initially empty habitat can be tracked directly. Using fluorescence microscopy, we follow the fate of individual Escherichia coli bacterial cell lineages as they undergo expansion competition (the race to be the first to colonize a previously empty territory), and as they later compete ...[more]

PMID: 26333814

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Project description:Understanding the factors that facilitate or constrain establishment of populations in novel environments is crucial for conservation biology and the study of adaptive radiation. Important questions include: (1) Does the timing of colonization relative to stochastic events, such as climatic perturbations, impact the probability of successful establishment? (2) To what extent does community context (e.g., the presence of competitors) change the probability of establishment? (3) How do sources of intrapopulation variance, such as sex differences, affect success at an individual level during the process of establishment? Answers to these questions are rarely pursued in a field-experimental context or on the same time scales (months to years) as the processes of colonization and establishment. We introduced slender anole lizards (Anolis apletophallus) to eight islands in the Panama Canal and tracked them over multiple generations to investigate the factors that mediate establishment success. All islands were warmer than the mainland (ancestral) environment, and some islands had a native competitor. We transplanted half of these populations only 4 months before the onset of a severe regional drought and the other half 2 years (two generations) before the drought. We found that successful establishment depended on both the intensity of interspecific competition and the timing of colonization relative to the drought. The islands that were colonized shortly before the drought went functionally extinct by the second generation, and regardless of time before the drought, the populations on islands with interspecific competition declined continuously over the study period. Furthermore, the effect of the competitor interacted with sex, with males suffering, and females benefitting, from the presence of a native competitor. Our results reveal that community context and the timing of colonization relative to climactic events can combine to determine establishment success and that these factors can generate opposite effects on males and females.

Project description:UNLABELLED:We recently showed that human gut Bacteroidales species secrete antimicrobial proteins (BSAPs), and we characterized in vitro the first such BSAP produced by Bacteroides fragilis In this study, we identified a second potent BSAP produced by the ubiquitous and abundant human gut species Bacteroides uniformis The two BSAPs contain a membrane attack complex/perforin (MACPF) domain but share very little sequence similarity. We identified the target molecules of BSAP-sensitive cells and showed that each BSAP targets a different class of surface molecule: BSAP-1 targets an outer membrane protein of sensitive B. fragilis strains, and BSAP-2 targets the O-antigen glycan of lipopolysaccharide (LPS) of sensitive B. uniformis strains. Species-wide genomic and phenotypic analyses of B. fragilis and B. uniformis showed that BSAP-producing strains circumvent killing by synthesizing an orthologous nontargeted surface molecule. The BSAP genes are adjacent to the gene(s) encoding their target replacements, suggesting coacquisition. Using a gnotobiotic mouse competitive-colonization model, we found that the BSAP surface targets are important for colonization of the mammalian gut, thereby explaining why they are maintained in sensitive strains and why they were replaced rather than deleted in BSAP-producing strains. Using isogenic BSAP-producing, -sensitive, and -resistant strains, we show that a BSAP-producing strain outcompetes a sensitive strain but not a resistant strain in the mammalian gut. Human gut metagenomic datasets reveal that BSAP-1-sensitive strains do not cooccur with BSAP-1-producing strains in human gut microbiotas, further supporting the idea that BSAPs are important competitive factors with relevance to the strain-level composition of the human gut microbiota. IMPORTANCE:We know relatively little about the ecology of the human intestinal microbiota and the combination of factors that dictate which strains and species occupy an individual's gut microbial community. Interference competition, mediated by bacterial factors that directly harm other members, is beginning to be appreciated as important in contributing to species- and strain-level dynamics of abundant gut bacteria. Here, we show that gut Bacteroidales secrete antimicrobial proteins (BSAPs) that antagonize strains of the same species. We show that BSAPs target molecules of sensitive cells that are important for gut colonization and therefore are maintained in sensitive cells. In an experimental animal model of gut colonization, a BSAP-1-producing strain antagonized and outcompeted an isogenic sensitive strain. Furthermore, metagenomic analyses showed that BSAP-1-producing and -sensitive strains are not found together in human gut microbiotas. These data suggest that BSAPs are strong ecological drivers shaping the strain-level composition of gut communities.

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Competition for space during bacterial colonization of a surface.

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Competition for space during bacterial colonization of a surface.

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