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

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 unculturedDesulfobulbus 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 byD. 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. Animal-associated microbiota likely assembled as a result of numerous independent colonization events by free-living microbes followed bymore » 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.« less
Authors:
 [1] ;  [1] ;  [2] ; ORCiD logo [3] ;  [1] ;  [2] ;  [3] ; ORCiD logo [2] ;  [1] ;  [2] ;  [3] ;  [2] ; ORCiD logo [1] ;  [3] ;  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. The Ohio State Univ., Columbus, OH (United States)
Publication Date:
Grant/Contract Number:
AC05-00OR22725
Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 9; Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Research Org:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org:
USDOE
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES
OSTI Identifier:
1435265

Cross, Karissa L., Chirania, Payal, Xiong, Weili, Beall, Clifford J., Elkins, James G., Giannone, Richard J., Griffen, Ann L., Guss, Adam M., Hettich, Robert L., Joshi, Snehal S., Mokrzan, Elaine M., Martin, Roman K., Zhulin, Igor B., Leys, Eugene J., and Podar, Mircea. Insights into the Evolution of Host Association through the Isolation and Characterization of a Novel Human Periodontal Pathobiont, Desulfobulbus oralis. United States: N. p., Web. doi:10.1128/mBio.02061-17.
Cross, Karissa L., Chirania, Payal, Xiong, Weili, Beall, Clifford J., Elkins, James G., Giannone, Richard J., Griffen, Ann L., Guss, Adam M., Hettich, Robert L., Joshi, Snehal S., Mokrzan, Elaine M., Martin, Roman K., Zhulin, Igor B., Leys, Eugene J., & Podar, Mircea. Insights into the Evolution of Host Association through the Isolation and Characterization of a Novel Human Periodontal Pathobiont, Desulfobulbus oralis. United States. doi:10.1128/mBio.02061-17.
Cross, Karissa L., Chirania, Payal, Xiong, Weili, Beall, Clifford J., Elkins, James G., Giannone, Richard J., Griffen, Ann L., Guss, Adam M., Hettich, Robert L., Joshi, Snehal S., Mokrzan, Elaine M., Martin, Roman K., Zhulin, Igor B., Leys, Eugene J., and Podar, Mircea. 2018. "Insights into the Evolution of Host Association through the Isolation and Characterization of a Novel Human Periodontal Pathobiont, Desulfobulbus oralis". United States. doi:10.1128/mBio.02061-17.
@article{osti_1435265,
title = {Insights into the Evolution of Host Association through the Isolation and Characterization of a Novel Human Periodontal Pathobiont, Desulfobulbus oralis},
author = {Cross, Karissa L. and Chirania, Payal and Xiong, Weili and Beall, Clifford J. and Elkins, James G. and Giannone, Richard J. and Griffen, Ann L. and Guss, Adam M. and Hettich, Robert L. and Joshi, Snehal S. and Mokrzan, Elaine M. and Martin, Roman K. and Zhulin, Igor B. and Leys, Eugene J. and Podar, Mircea},
abstractNote = {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 unculturedDesulfobulbus 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 byD. 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. 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.},
doi = {10.1128/mBio.02061-17},
journal = {mBio (Online)},
number = 2,
volume = 9,
place = {United States},
year = {2018},
month = {3}
}

Works referenced in this record:

The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013

Microbial complexes in subgingival plaque
journal, February 1998