Division of Infectious Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, United States of America.
PLoS Genet. 2021 Apr 26;17(4):e1009541. doi: 10.1371/journal.pgen.1009541. eCollection 2021 Apr.
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.
人类肠道微生物群是一个密集的微生物生态系统，为细菌接触依赖性过程提供了广泛的机会，例如共轭和类型 VI 分泌系统（T6SS）依赖性拮抗作用。在肠道拟杆菌目中，T6SS 基因座的两个不同的遗传结构，GA1 和 GA2，包含在整合和共轭元件（ICE）上。尽管人们对肠道拟杆菌目中的 T6SS 非常感兴趣，但对其进化模式以及它们在人类肠道群落中拟杆菌目中的传播知之甚少。在这里，我们结合广泛的基因组和宏基因组分析来更好地了解它们的生态和进化动态。我们确定了新的遗传亚型，记录了这些 ICE 在人类肠道微生物组内的拟杆菌目中的广泛个体间转移，最重要的是，揭示了这些新武装菌株在一个人内的多个物种中频繁的种群固定。我们进一步展示了每种不同的 T6SS 在人类群体中的分布，并显示出存在地理聚类。我们揭示了 GA1 T6SS ICE 整合在最小重组位点，导致它们在整个基因组中整合并经常中断基因，而 GA2 T6SS ICE 整合在三个不同 tRNA 基因之一。在单个菌株中排除同时存在的 GA1 和 GA2 T6SS 与完整的 T6SS 基因座和 ICE 编码基因有关。通过对许多人类肠道群落中同居的拟杆菌目中的移动遗传元件（MGE）进行全面分析，我们确定了 74 个 MGE 转移到单个肠道微生物组内的多个拟杆菌目中。我们进一步表明，只有其他三个 MGE 在人类肠道微生物组中表现出与 GA1 和 GA2 ICE 相同程度的多物种传播。这些数据强调了移动 T6SS 基因座在拟杆菌目中的普遍性和传播性以及在人类群体中的传播性。
