Background: The increasing availability of microbial genomes and environmental shotgun metagenomes provides unprecedented access to the genomic differences within related bacteria. The human oral microbiome with its diverse habitats and abundant, relatively well-characterized microbial inhabitants presents an opportunity to investigate bacterial population structures at an ecosystem scale. Results: Here, we employ a metapangenomic approach that combines public genomes with Human Microbiome Project (HMP) metagenomes to study the diversity of microbial residents of three oral habitats: tongue dorsum, buccal mucosa, and supragingival plaque. For two exemplar taxa, Haemophilus parainfluenzae and the genus Rothia, metapangenomes revealed distinct genomic groups based on shared genome content. H. parainfluenzae genomes separated into three distinct subgroups with differential abundance between oral habitats. Functional enrichment analyses identified an operon encoding oxaloacetate decarboxylase as diagnostic for the tongue-abundant subgroup. For the genus Rothia, grouping by shared genome content recapitulated species-level taxonomy and habitat preferences. However, while most R. mucilaginosa were restricted to the tongue as expected, two genomes represented a cryptic population of R. mucilaginosa in many buccal mucosa samples. For both H. parainfluenzae and the genus Rothia, we identified not only limitations in the ability of cultivated organisms to represent populations in their native environment, but also specifically which cultivar gene sequences were absent or ubiquitous. Conclusions: Our findings provide insights into population structure and biogeography in the mouth and form specific hypotheses about habitat adaptation. These results illustrate the power of combining metagenomes and pangenomes to investigate the ecology and evolution of bacteria across analytical scales.

中文翻译：

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口腔微生物组的超基因组学提供了有关栖息地适应和品种多样性的见解

背景：微生物基因组和环境shot弹枪基因组的可用性不断提高，提供了前所未有的途径来获得相关细菌内的基因组差异。具有多种多样的栖息地和相对丰富的微生物种群的人类口腔微生物组为研究生态系统规模的细菌种群结构提供了机会。结果：在这里，我们采用了一种将人类基因组计划与人类微生物组计划（HMP）的基因组相结合的超基因组学方法，研究了三种口腔栖息地的微生物种群的多样性：舌背，颊黏膜和龈上菌斑。对于两个典型的类群，副流感嗜血杆菌和Rothia属，超基因组学基于共有的基因组含量揭示了不同的基因组。副流感嗜血杆菌基因组分为三个不同的亚组，口腔生境之间的丰度差异很大。功能富集分析确定了编码草酰乙酸脱羧酶的操纵子，可诊断出舌头丰富的亚组。对于Rothia属，按共享的基因组含量分组概括了物种级分类法和生境偏好。但是，尽管大多数粘液鼠李菌如预期的那样只限于舌头，在许多颊粘膜样品中，两个基因组代表了粘液隐球菌的隐居种群。对于副流感嗜血杆菌和Rothia属，我们不仅确定了栽培有机物代表其原生环境中种群的能力的局限性，而且还明确了缺少或普遍存在的哪个品种基因序列。结论：我们的发现提供了对口中种群结构和生物地理学的见解，并形成了有关生境适应性的特定假设。这些结果说明了结合基因组和全基因组研究跨分析规模的细菌的生态学和进化的力量。