Insights into the Evolution of Host Association through the Isolation and Characterization of a Novel Human Periodontal Pathobiont,Desulfobulbus oralis

Abstract

The human oral microbiota encompasses representatives of many bacterial lineages that have not yet been cultured. Here we describe the isolation and characterization of previously uncultured Desulfobulbus oralis, the first humanassociated representative of its genus. As mammalian-associated microbes rarely have free-living close relatives, D. oralis provides opportunities to study how bacteria adapt and evolve within a host. This sulfate-reducing deltaproteobacterium has adapted to the human oral subgingival niche by curtailing its physiological repertoire, losing some biosynthetic abilities and metabolic independence, and by dramatically reducing environmental sensing and signaling capabilities. The genes that enable free-living Desulfobulbus to synthesize the potent neurotoxin methylmercury were also lost by D. oralis, a notably positive outcome of host association. However, horizontal gene acquisitions from other members of the microbiota provided novel mechanisms of interaction with the human host, including toxins like leukotoxin and hemolysins. Proteomic and transcriptomic analysis revealed that most of those factors are actively expressed, including in the subgingival environment, and some are secreted. Similar to other known oral pathobionts, D. oralis can trigger a proinflammatory response in oral epithelial cells, suggesting a direct role in the development of periodontal disease.IMPORTANCE Animal-associated microbiota likely assembled as a result of numerous independent colonization events by free-living microbes followed by coevolution with their host and other microbes. Through specific adaptation to various body sites and physiological niches, microbes have a wide range of contributions, from beneficial to disease causing. Desulfobulbus oralis provides insights into genomic and physiological transformations associated with transition from an open environment to a host-dependent lifestyle and the emergence of pathogenicity. Through a multifaceted mechanism triggering a proinflammatory response, D. oralis is a novel periodontal pathobiont. Even though culture-independent approaches can provide insights into the potential role of the human microbiome "dark matter," cultivation and experimental characterization remain important to studying the roles of individual organisms in health and disease.KEYWORDS evolution, genome analysis, oral microbiology, periodontitis, proteomics

Microbial differences between dental plaque and historic dental calculus are related to oral biofilm maturation stage

“…2b) and that contribute to the classification of historic samples compared to plaque (Additional file 1: Figure S5D), including C. rectus , Desulfobulbus sp. oral taxon 041 (aka Desulfobulbus oralis [26]), and F. alocis (Additional file 1: Figure S7B,C).

Fig. 4Modern and historic calculus microbial community profiles overlap.

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Review: modulation of the oral microbiome by the host to promote ecological balance

“…It has been proposed that the oral microbiota stayed relatively stable until major dietary changes during the history of human evolution, which induced a compositional shift along with a noticeable decrease in its diversity [4]. Moreover, adaptation of bacteria to these new environmental conditions [5, 6] and continuous changes in the environment and lifestyle of the host [7] are believed to have greatly contributed to the present configuration of the oral microbiome in humans.…”

The Postmedieval Latvian Oral Microbiome in the Context of Modern Dental Calculus and Modern Dental Plaque Microbial Profiles

“…The most abundant bacterial taxa detected in our historical calculus samples included several commensal bacterial species that are commonly found in the human oral cavity, such as Streptococcus sanguinis , Streptococcus cristatus and Lautropia mirabilis . The periodontal pathobiont Desulfobulbus oralis was present among the 10 most abundant bacterial species from postmedieval dental calculus samples, which is known for its ability to trigger a proinflammatory response in the oral epithelium [ 44 ]. Additionally, many oral pathogens that are involved in the etiology of caries, such as Streptococcus mutans , or periodontal disease, including three Gram-negative species known as the ‘red-complex’— Porphyromonas gingivalis , Tannerella forsythia , and Treponema denticola —were detected in our historical calculus samples.…”