The human gut microbiota is a dense microbial ecosystem with extensive opportunities for bacterial contact-dependent processes such as conjugation and Type VI secretion system (T6SS)-dependent antagonism. In the gut Bacteroidales, two distinct genetic architectures of T6SS loci, GA1 and GA2, are contained on Integrative and Conjugative Elements (ICE). Despite intense interest in the T6SSs of the gut Bacteroidales, there is only a superficial understanding of their evolutionary patterns, and of their dissemination among Bacteroidales species in human gut communities. Here, we combine extensive genomic and metagenomic analyses to better understand their ecological and evolutionary dynamics. We identify new genetic subtypes, document extensive intrapersonal transfer of these ICE to Bacteroidales species within human gut microbiomes, and most importantly, reveal frequent population fixation of these newly armed strains in multiple species within a person. We further show the distribution of each of the distinct T6SSs in human populations and show there is geographical clustering. We reveal that the GA1 T6SS ICE integrates at a minimal recombination site leading to their integration throughout genomes and their frequent interruption of genes, whereas the GA2 T6SS ICE integrate at one of three different tRNA genes. The exclusion of concurrent GA1 and GA2 T6SSs in individual strains is associated with intact T6SS loci and with an ICE-encoded gene. By performing a comprehensive analysis of mobile genetic elements (MGE) in co-resident Bacteroidales species in numerous human gut communities, we identify 74 MGE that transferred to multiple Bacteroidales species within individual gut microbiomes. We further show that only three other MGE demonstrate multi-species spread in human gut microbiomes to the degree demonstrated by the GA1 and GA2 ICE. These data underscore the ubiquity and dissemination of mobile T6SS loci within Bacteroidales communities and across human populations. Author summary Bacteroidales are abundant members of the gut microbiota of human populations across the globe. Bacteroidales use Type VI secretion systems (T6SS) to deliver toxins to neighboring cells to gain a competitive advantage. Bacteroidales T6SS are of three different genetic architectures, two of which are contained on mobile genetic elements (MGEs). Due to the phenotypes conferred by cargo genes contained on MGE, their dissemination greatly impacts the ecology and evolution of human gut microbial communities. Here, we present a comprehensive analysis of the prevalence and dissemination of these mobile T6SS loci in gut Bacteroidales species across human populations. We reveal extensive dissemination of T6SS loci to numerous Bacteroidales species in human gut microbiomes with these newly armed strains outcompeting their progenitors. Few other Bacteroidales MGE spread in as many human communities to the degree detected for the T6SS MGEs. Considering the expected cost associated with maintaining these MGEs, these observations suggest that their acquisition confers a significant benefit, increasing fitness of individual strains and possibly the Bacteroidales community as a whole.
【초록키워드】 Evolution, Genome, Genetic, Spread, Prevalence, Impact, Microbiome, Clustering, Recombination, Community, phenotype, evolutionary dynamics, gut microbiota, genomes, fitness, dissemination, distribution, genomic, Bacterial, Analysis, strain, Gut, fixation, microbial, human populations, human population, tRNA, Ecology, observation, Phenotypes, Subtypes, competitive advantage, comprehensive analysis, These data, species, secretion, transfer, multi, exclusion, loci, acquisition, element, genetic architecture, toxin, toxins, Bacteroidales, conjugation, metagenomic analyses, neighboring cells, Genes, benefit, identify, globe, demonstrated, expected, Type, ecological, Bacteroidale, metagenomic, microbial ecosystem, neighboring cell, transferred, 【제목키워드】 Spread, Clustering, Gut, secretion, transfer, loci, Type, Bacteroidale, Mobile,