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Comparative genomics of human Lactobacillus crispatus isolates reveals genes for glycosylation and glycogen degradation: implications for in vivo dominance of the vaginal microbiota.

ABSTRACT: BACKGROUND:A vaginal microbiota dominated by lactobacilli (particularly Lactobacillus crispatus) is associated with vaginal health, whereas a vaginal microbiota not dominated by lactobacilli is considered dysbiotic. Here we investigated whether L. crispatus strains isolated from the vaginal tract of women with Lactobacillus-dominated vaginal microbiota (LVM) are pheno- or genotypically distinct from L. crispatus strains isolated from vaginal samples with dysbiotic vaginal microbiota (DVM). RESULTS:We studied 33?L. crispatus strains (n?=?16 from LVM; n?=?17 from DVM). Comparison of these two groups of strains showed that, although strain differences existed, both groups degraded various carbohydrates, produced similar amounts of organic acids, inhibited Neisseria gonorrhoeae growth, and did not produce biofilms. Comparative genomics analyses of 28 strains (n?=?12 LVM; n?=?16 DVM) revealed a novel, 3-fragmented glycosyltransferase gene that was more prevalent among strains isolated from DVM. Most L. crispatus strains showed growth on glycogen-supplemented growth media. Strains that showed less-efficient (n?=?6) or no (n?=?1) growth on glycogen all carried N-terminal deletions (respectively, 29 and 37 amino acid deletions) in a putative pullulanase type I protein. DISCUSSION:L. crispatus strains isolated from LVM were not phenotypically distinct from L. crispatus strains isolated from DVM; however, the finding that the latter were more likely to carry a 3-fragmented glycosyltransferase gene may indicate a role for cell surface glycoconjugates, which may shape vaginal microbiota-host interactions. Furthermore, the observation that variation in the pullulanase type I gene is associated with growth on glycogen discourages previous claims that L. crispatus cannot directly utilize glycogen.

SUBMITTER: van der Veer C

PROVIDER: S-EPMC6441167 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Comparative genomics of human Lactobacillus crispatus isolates reveals genes for glycosylation and glycogen degradation: implications for in vivo dominance of the vaginal microbiota.

van der Veer Charlotte C Hertzberger Rosanne Y RY Bruisten Sylvia M SM Tytgat Hanne L P HLP Swanenburg Jorne J de Kat Angelino-Bart Alie A Schuren Frank F Molenaar Douwe D Reid Gregor G de Vries Henry H Kort Remco R

Microbiome 20190329 1

<h4>Background</h4>A vaginal microbiota dominated by lactobacilli (particularly Lactobacillus crispatus) is associated with vaginal health, whereas a vaginal microbiota not dominated by lactobacilli is considered dysbiotic. Here we investigated whether L. crispatus strains isolated from the vaginal tract of women with Lactobacillus-dominated vaginal microbiota (LVM) are pheno- or genotypically distinct from L. crispatus strains isolated from vaginal samples with dysbiotic vaginal microbiota (DVM ...[more]

PMID: 30925932

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Project description:BackgroundLactobacillus crispatus is the dominant species in the vaginal microbiota associated with health and considered a homeostasis biomarker. Interestingly, some strains are even used as probiotics. However, the genetic mechanisms of L. crispatus involved in the control of the vaginal microbiome and protection against bacterial vaginosis (BV) are not entirely known. To further investigate these mechanisms, we sequenced and characterized the first four L. crispatus genomes from vaginal samples from Brazilian women and used genome-wide association study (GWAS) and comparative analyses to identify genetic mechanisms involved in healthy or BV conditions and selective pressures acting in the vaginal microbiome.MethodsThe four genomes were sequenced, assembled using ten different strategies and automatically annotated. The functional characterization was performed by bioinformatics tools comparing with known probiotic strains. Moreover, it was selected one representative strain (L. crispatus CRI4) for in vitro detection of phages by electron microscopy. Evolutionary analysis, including phylogeny, GWAS and positive selection were performed using 46 public genomes strains representing health and BV conditions.ResultsGenes involved in probiotic effects such as lactic acid production, hydrogen peroxide, bacteriocins, and adhesin were identified. Three hemolysins and putrescine production were predicted, although these features are also present in other probiotic strains. The four genomes presented no plasmids, but 14 known families insertion sequences and several prophages were detected. However, none of the mobile genetic elements contained antimicrobial resistance genes. The genomes harbor a CRISPR-Cas subtype II-A system that is probably inactivated due to fragmentation of the genes csn2 and cas9. No genomic feature was associated with a health condition, perhaps due to its multifactorial characteristic. Five genes were identified as under positive selection, but the selective pressure remains to be discovered. In conclusion, the Brazilian strains investigated in this study present potential protective properties, although in vitro and in vivo studies are required to confirm their efficacy and safety to be considered for human use.

Project description:Bacterial communities colonizing the reproductive tracts of primates (including humans) impact the health, survival and fitness of the host, and thereby the evolution of the host species. Despite their importance, we currently have a poor understanding of primate microbiomes. The composition and structure of microbial communities vary considerably depending on the host and environmental factors. We conducted comparative analyses of the primate vaginal microbiome using pyrosequencing of the 16S rRNA genes of a phylogenetically broad range of primates to test for factors affecting the diversity of primate vaginal ecosystems. The nine primate species included: humans (Homo sapiens), yellow baboons (Papio cynocephalus), olive baboons (Papio anubis), lemurs (Propithecus diadema), howler monkeys (Alouatta pigra), red colobus (Piliocolobus rufomitratus), vervets (Chlorocebus aethiops), mangabeys (Cercocebus atys) and chimpanzees (Pan troglodytes). Our results indicated that all primates exhibited host-specific vaginal microbiota and that humans were distinct from other primates in both microbiome composition and diversity. In contrast to the gut microbiome, the vaginal microbiome showed limited congruence with host phylogeny, and neither captivity nor diet elicited substantial effects on the vaginal microbiomes of primates. Permutational multivariate analysis of variance and Wilcoxon tests revealed correlations among vaginal microbiota and host species-specific socioecological factors, particularly related to sexuality, including: female promiscuity, baculum length, gestation time, mating group size and neonatal birth weight. The proportion of unclassified taxa observed in nonhuman primate samples increased with phylogenetic distance from humans, indicative of the existence of previously unrecognized microbial taxa. These findings contribute to our understanding of host-microbe variation and coevolution, microbial biogeography, and disease risk, and have important implications for the use of animal models in studies of human sexual and reproductive diseases.

Dataset Information

Comparative genomics of human Lactobacillus crispatus isolates reveals genes for glycosylation and glycogen degradation: implications for in vivo dominance of the vaginal microbiota.

Publications

Comparative genomics of human Lactobacillus crispatus isolates reveals genes for glycosylation and glycogen degradation: implications for in vivo dominance of the vaginal microbiota.

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