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Dispersal strategies shape persistence and evolution of human gut bacteria.

ABSTRACT: Human gut bacterial strains can co-exist with their hosts for decades, but little is known about how these microbes persist and disperse, and evolve thereby. Here, we examined these processes in 5,278 adult and infant fecal metagenomes, longitudinally sampled in individuals and families. Our analyses revealed that a subset of gut species is extremely persistent in individuals, families, and geographic regions, represented often by locally successful strains of the phylum Bacteroidota. These "tenacious" bacteria show high levels of genetic adaptation to the human host but a high probability of loss upon antibiotic interventions. By contrast, heredipersistent bacteria, notably Firmicutes, often rely on dispersal strategies with weak phylogeographic patterns but strong family transmissions, likely related to sporulation. These analyses describe how different dispersal strategies can lead to the long-term persistence of human gut microbes with implications for gut flora modulations.

SUBMITTER: Hildebrand F

PROVIDER: S-EPMC8288446 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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Dispersal strategies shape persistence and evolution of human gut bacteria.

Hildebrand Falk F Gossmann Toni I TI Frioux Clémence C Özkurt Ezgi E Myers Pernille Neve PN Ferretti Pamela P Kuhn Michael M Bahram Mohammad M Nielsen Henrik Bjørn HB Bork Peer P

Cell host & microbe 20210609 7

Human gut bacterial strains can co-exist with their hosts for decades, but little is known about how these microbes persist and disperse, and evolve thereby. Here, we examined these processes in 5,278 adult and infant fecal metagenomes, longitudinally sampled in individuals and families. Our analyses revealed that a subset of gut species is extremely persistent in individuals, families, and geographic regions, represented often by locally successful strains of the phylum Bacteroidota. These "ten ...[more]

PMID: 34111423

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Project description:BackgroundConsiderable attention has focused on how selection on dispersal and other core life-history strategies (reproductive effort, survival ability, colonization capacity) may lead to so-called dispersal syndromes. Studies on genetic variation in these syndromes within species could importantly increase our understanding of their evolution, by revealing whether traits co-vary across genetic lineages in the manner predicted by theoretical models, and by stimulating further hypotheses for experimental testing. Yet such studies remain scarce. Here we studied the ciliated protist Tetrahymena thermophila, a particularly interesting organism due to cells being able to transform into morphs differing dramatically in swim-speed. We investigated dispersal, morphological responses, reproductive performance, and survival in ten different clonal strains. Then, we examined whether life history traits co-varied in the manner classically predicted for ruderal species, examined the investment of different strains into short- and putative long-distance dispersal, while considering also the likely impact of semi-sociality (cell aggregation, secretion of 'growth factors') on dispersal strategies.ResultsVery significant among-strain differences were found with regard to dispersal rate, morphological commitment and plasticity, and almost all core life-history traits (e.g. survival, growth performance and strategy), with most of these traits being significantly intercorrelated. Some strains showed high short-distance dispersal rates, high colonization capacity, bigger cell size, elevated growth performance, and good survival abilities. These well performing strains, however, produced fewer fast-swimming dispersal morphs when subjected to environmental degradation than did philopatric strains performing poorly under normal conditions.ConclusionStrong evidence was found for a genetic covariation between dispersal strategies and core life history traits in T. thermophila, with a fair fit of observed trait associations with classic colonizer models. However, the well performing strains with high colonization success and short-distance dispersal likely suffered under a long-distance dispersal disadvantage, due to producing fewer fast-swimming dispersal morphs than did philopatric strains. The smaller cell size at carrying capacity of the latter strains and their poor capacity to colonize as individual cells suggest that they may be adapted to greater levels of dependency on clone-mates (stronger sociality). In summary, differential exposure to selection on competitive and cooperative abilities, in conjunction with selective factors targeting specifically dispersal distance, likely contributed importantly to shaping T. thermophila dispersal and life history evolution.

Project description:Background and aimsIsolated populations constitute an ideal laboratory to study the consequences of intraspecific divergence, because intrinsic incompatibilities are more likely to accumulate under reduced gene flow. Here, we use a widespread bromeliad with a patchy distribution, Pitcairnia lanuginosa, as a model to infer processes driving Neotropical diversification and, thus, to improve our understanding of the origin and evolutionary dynamics of biodiversity in this highly speciose region.MethodsWe assessed the timing of lineage divergence, genetic structural patterns and historical demography of P. lanuginosa, based on microsatellites, and plastid and nuclear sequence data sets using coalescent analyses and an Approximate Bayesian Computation framework. Additionally, we used species distribution models (SDMs) to independently estimate potential changes in habitat suitability.Key resultsDespite morphological uniformity, plastid and nuclear DNA data revealed two distinct P. lanuginosa lineages that probably diverged through dispersal from the Cerrado to the Central Andean Yungas, following the final uplift of the Andes, and passed through long-term isolation with no evidence of migration. Microsatellite data indicate low genetic diversity and high levels of inbreeding within populations, and restricted gene flow among populations, which are likely to be a consequence of bottlenecks (or founder events), and high selfing rates promoting population persistence in isolation. SDMs showed a slight expansion of the suitable range for P. lanuginosa lineages during the Last Glacial Maximum, although molecular data revealed a signature of older divergence. Pleistocene climatic oscillations thus seem to have played only a minor role in the diversification of P. lanuginosa, which probably persisted through adverse conditions in riparian forests.ConclusionsOur results imply drift as a major force shaping the evolution of P. lanuginosa, and suggest that dispersal events have a prominent role in connecting Neotropical open and forest biomes.

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Dispersal strategies shape persistence and evolution of human gut bacteria.

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Dispersal strategies shape persistence and evolution of human gut bacteria.

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