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Slipped-Strand Mispairing in the Gene Encoding Sialidase NanH3 in Gardnerella spp.

ABSTRACT: Cell wall proteins with sialidase activity are involved in carbohydrate assimilation, adhesion to mucosal surfaces, and biofilm formation. Gardnerella spp. inhabit the human vaginal microbiome and encode up to three sialidase enzymes, two of which are suspected to be cell wall associated. Here, we demonstrate that the gene encoding extracellular sialidase NanH3 is found almost exclusively in Gardnerella piotii and the closely related species Gardnerella genome sp. 3, and its presence correlates with a sialidase-positive phenotype in a collection of 112 Gardnerella isolates. The nanH3 gene sequence includes a homopolymeric repeat of cytosines that varies in length within cell populations, indicating that this gene is subject to slipped-strand mispairing, a mechanism of phase variation in bacteria. Variation in the length of the homopolymer sequence results in production of either the full-length sialidase protein or truncated peptides lacking the sialidase domain due to introduction of reading-frame shifts and premature stop codons. Phase variation in NanH3 may be involved in immune evasion or modulation of adhesion to host epithelial cells and formation of biofilms characteristic of the vaginal dysbiosis known as bacterial vaginosis.

SUBMITTER: Kurukulasuriya SP

PROVIDER: S-EPMC8097274 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Gardnerella spp. are pathognomonic for bacterial vaginosis, which increases the risk of preterm birth and the transmission of sexually transmitted infections. Gardnerella spp. are genetically diverse, comprising what have recently been defined as distinct species with differing functional capacities. Disease associations with Gardnerella spp. are not straightforward: patients with BV are usually infected with multiple species, and Gardnerella spp. are also found in the vaginal microbiome of healthy women. Genome comparisons of Gardnerella spp. show evidence of lateral gene transfer (LGT), but patterns of LGT have not been characterized in detail. Here we sought to define the role of LGT in shaping the genetic structure of Gardnerella spp. We analyzed whole genome sequencing data for 106 Gardnerella strains and used these data for pan genome analysis and to characterize LGT in the core and accessory genomes, over recent and remote timescales. In our diverse sample of Gardnerella strains, we found that both the core and accessory genomes are clearly differentiated in accordance with newly defined species designations. We identified putative competence and pilus assembly genes across most species; we also found them to be differentiated between species. Competence machinery has diverged in parallel with the core genome, with selection against deleterious mutations as a predominant influence on their evolution. By contrast, the virulence factor vaginolysin, which encodes a toxin, appears to be readily exchanged among species. We identified five distinct prophage clusters in Gardnerella genomes, two of which appear to be exchanged between Gardnerella species. Differences among species are apparent in their patterns of LGT, including their exchange with diverse gene pools. Despite frequent LGT and co-localization in the same niche, our results show that Gardnerella spp. are clearly genetically differentiated and yet capable of exchanging specific genetic material. This likely reflects complex interactions within bacterial communities associated with the vaginal microbiome. Our results provide insight into how such interactions evolve and are maintained, allowing these multi-species communities to colonize and invade human tissues and adapt to antibiotics and other stressors.

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Slipped-Strand Mispairing in the Gene Encoding Sialidase NanH3 in Gardnerella spp.

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