Abundance and co-occurrence of extracellular capsules increase environmental breadth: Implications for the emergence of pathogens

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Rendueles, Olaya | Garcia-Garcerà, Marc | Néron, Bertrand | Touchon, Marie | Rocha, Eduardo, P C

Edité par CCSD ; Public Library of Science -

International audience. Extracellular capsules constitute the outermost layer of many bacteria, are major virulencefactors, and affect antimicrobial therapies. They have been used as epidemiological markersand recently became vaccination targets. Despite the efforts to biochemically serotypecapsules in a few model pathogens, little is known of their taxonomic and environmental distribution.We developed, validated, and made available a computational tool, CapsuleFinder,to identify capsules in genomes. The analysis of over 2500 prokaryotic genomes,accessible in a database, revealed that ca. 50% of them - including ArchaeaÐencode acapsule. The Wzx/Wzy-dependent capsular group was by far the most abundant. Surprisingly,a fifth of the genomes encode more than one capsule system, often from differentgroups, and their non-random co-occurrence suggests the existence of negative and positiveepistatic interactions. To understand the role of multiple capsules, we queried morethan 6700 metagenomes for the presence of species encoding capsules and showed thattheir distribution varied between environmental categories and, within the human microbiome,between body locations. Species encoding capsules, and especially those encodingmultiple capsules, had larger environmental breadths than the other species. Accordingly,capsules were more frequent in environmental bacteria than in pathogens and, within thelatter, they were more frequent among facultative pathogens. Nevertheless, capsules werefrequent in clinical samples, and were usually associated with fast-growing bacteria withhigh infectious doses. Our results suggest that capsules increase the environmental rangeof bacteria and make them more resilient to environmental perturbations. Capsules mightallow opportunistic pathogens to profit from empty ecological niches or environmental perturbations,such as those resulting from antibiotic therapy, to colonize the host. Capsule-associatedvirulence might thus be a by-product of environmental adaptation. Understandingthe role of capsules in natural environments might enlighten their function inpathogenesis.

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