Abstract

Extracellular capsules constitute the outermost layer of many bacteria, are major virulence factors, and affect antimicrobial therapies. They have been used as epidemiological markers and recently became vaccination targets. Despite the efforts to biochemically serotype capsules 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 Archaea—encode a capsule. 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 different groups—and their non-random co-occurrence suggests the existence of negative and positive epistatic interactions. To understand the role of multiple capsules, we queried more than 6700 metagenomes for the presence of species encoding capsules and showed that their distribution varied between environmental categories and, within the human microbiome, between body locations. Species encoding capsules, and especially those encoding multiple capsules, had larger environmental breadths than the other species. Accordingly, capsules were more frequent in environmental bacteria than in pathogens and, within the latter, they were more frequent among facultative pathogens. Nevertheless, capsules were frequent in clinical samples, and were usually associated with fast-growing bacteria with high infectious doses. Our results suggest that capsules increase the environmental range of bacteria and make them more resilient to environmental perturbations. Capsules might allow opportunistic pathogens to profit from empty ecological niches or environmental perturbations, such as those resulting from antibiotic therapy, to colonize the host. Capsule-associated virulence might thus be a by-product of environmental adaptation. Understanding the role of capsules in natural environments might enlighten their function in pathogenesis.

Highlights

  • Extracellular capsules, hereafter named capsules, constitute the outermost layer of some prokaryotic cells where they establish the first contact between the microorganism and its environment

  • Since little was known about their frequency across Prokaryotes, we created and made freely available a computational tool, CapsuleFinder, to identify them from genomic data

  • Bacteria encoding capsule systems were found in many natural environments, and were frequent in the human microbiome

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Summary

Introduction

Extracellular capsules, hereafter named capsules, constitute the outermost layer of some prokaryotic cells where they establish the first contact between the microorganism and its environment. They fullfill a myriad of roles, often linked to colonization and persistence. Capsules reduce the efficiency of antibiotics [7] and cationic antimicrobial peptides [8] These medical implications have driven the research on capsules and their roles, leading to the widespread perception that they are mostly associated with virulence [9, 10]. This triggered the numerous studies on the genetic diversity of capsules in several prominent bacterial pathogens such as Streptococcus pneumoniae [11, 12], Escherichia coli [13], Klebsiella pneumoniae [14, 15], Campylobacter jejuni [16], and Acinetobacter baumanii [17]

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