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

Karissa L Cross,Robert L Hettich,Adam M Guss,Richard J Giannone,Payal Chirania,Clifford J Beall,Eugene J Leys,Roman K Martin,James G Elkins,Ann L Griffen,Igor B Zhulin,Weili Xiong,Elaine M Mokrzan,Mircea Podar,Snehal S Joshi

doi:10.1128/mbio.02061-17

Abstract

ABSTRACTThe 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 human-associated 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.

Highlights

The human oral microbiota encompasses representatives of many bacterial lineages that have not yet been cultured
As with other oral species, it has remained unclear if those organisms play a role in the etiology of periodontitis or their increased abundance is a consequence of the disease state, with deep subgingival pockets favoring the proliferation of strict anaerobes
Isolation and Characterization of Desulfobulbus oralis oral subgingival samples collected from an individual with chronic periodontitis

Summary

Introduction

The human oral microbiota encompasses representatives of many bacterial lineages that have not yet been cultured. Desulfobulbus oralis has a reduced genome that displays limited conserved gene synteny compared to its closest sequenced free-living relative (Fig. 4), as well as evidence for both gene loss and gene gain.

Results

Conclusion