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Episymbiotic Saccharibacteria suppresses gingival inflammation and bone loss in mice through host bacterial modulation

Chipashvili, Otari and Utter, Daniel R. and Bedree, Joseph K. and Ma, Yansong and Schulte, Fabian and Mascarin, Gabrielle and Alayyoubi, Yasmin and Chouhan, Deepak and Hardt, Markus and Bidlack, Felicitas and Hasturk, Hatice and He, Xuesong and McLean, Jeffrey S. and Bor, Batbileg (2021) Episymbiotic Saccharibacteria suppresses gingival inflammation and bone loss in mice through host bacterial modulation. Cell Host and Microbe, 29 (11). pp. 1649-1662. ISSN 1931-3128. PMCID PMC8595704. doi:10.1016/j.chom.2021.09.009. https://resolver.caltech.edu/CaltechAUTHORS:20211022-170856506

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Abstract

Saccharibacteria (TM7) are obligate epibionts living on the surface of their host bacteria and are strongly correlated with dysbiotic microbiomes during periodontitis and other inflammatory diseases, suggesting they are putative pathogens. However, due to the recalcitrance of TM7 cultivation, causal research to investigate their role in inflammatory diseases is lacking. Here, we isolated multiple TM7 species on their host bacteria from periodontitis patients. These TM7 species reduce inflammation and consequential bone loss by modulating host bacterial pathogenicity in a mouse ligature-induced periodontitis model. Two host bacterial functions involved in collagen binding and utilization of eukaryotic sialic acid are required for inducing bone loss and are altered by TM7 association. This TM7-mediated downregulation of host bacterial pathogenicity is shown for multiple TM7/host bacteria pairs, suggesting that, in contrast to their suspected pathogenic role, TM7 could protect mammalian hosts from inflammatory damage induced by their host bacteria.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.chom.2021.09.009DOIArticle
https://doi.org/10.17632/vp68zv9wj9.1DOIData
http://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD026999Related ItemData
https://doi.org/10.6019/PXD026999DOIData
ORCID:
AuthorORCID
Chipashvili, Otari0000-0002-5454-2388
Utter, Daniel R.0000-0003-3322-7108
Bedree, Joseph K.0000-0002-3822-649X
Schulte, Fabian0000-0001-9047-2674
Hardt, Markus0000-0002-2300-216X
Bidlack, Felicitas0000-0001-8105-223X
Hasturk, Hatice0000-0002-4395-3958
He, Xuesong0000-0002-3333-9188
McLean, Jeffrey S.0000-0002-1797-1730
Bor, Batbileg0000-0002-1797-1730
Additional Information:© 2021 Elsevier Inc. Received 15 July 2021, Revised 23 August 2021, Accepted 16 September 2021, Available online 11 October 2021. We thank Xiaozhe Han and Yufeng Wang for ligature training; Alpdogan Kantarci, Thomas Van Dyke, and Ning Yu for productive discussion on immunology; Floyd Dewhirst and Mircea Podar for host bacterial strains. We also thank Jennifer Gundrum and Tabita Ramirez-Puebla for fluorescence imaging. We were supported by the National Institute of Dental and Craniofacial Research of the National Institutes of Health under awards 1R01DE023810, 1R01DE020102, 1R01DE026186 (to X.H., and J.S.M.); F31DE026057 (to J.K.B.); and 1K99DE027719-01 (to B.B.). Additional support was provided to D.R.U. by the National Science Foundation Graduate Research Fellowship Program under grant DGE1745303 (to D.R.U.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH or NSF. Preliminary studies were supported by the Forsyth Institute Pilot Grant Program. Data and code availability: The raw sequencing data and original code generated by this study were deposited on Mendeley Data: https://doi.org/10.17632/vp68zv9wj9.1, with the exception of initial 32 patient 16S rRNA sequencing data. These data were collected as a confidential medical record at Forsyth Center for Clinical and Translational Research, and we cannot release the raw data publicly due to ethical prohibition. Individuals who are interested in these data can contact the Lead Contact. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE [1] partner repository with the database identifiers: PXD026999 and 10.6019/PXD026999. Please see detailed discriptions of the data collection and analysis in STAR methods. Author contributions: Conceptualization, J.S.M., X.H., D.R.U., and B.B.; methodology, O.C., D.R.U., J.K.B., Y.M., F.S., Y.A., M.H., F.B., H.H., J.S.M., X.H., and B.B.; investigation, O.C., D.R.U., J.K.B., Y.M., F.S., G.M., Y.A., H.H., J.S.M., and B.B.; formal analysis, O.C., D.R.U., J.K.B., F.S., D.C., Y.A., F.B., M.H., J.S.M., X.H., and B.B.; writing – original draft, O.C., D.R.U., J.S.M., X.H., and B.B.; data curation, D.R.U., F.S., M.H., Y.A., H.H., and J.S.M.; writing – review & editing, all authors; project administration and funding acquisition, B.B., J.S., and X.H.; resources O.C., D.R.U., J.K.B., D.C., Y.M., F.S., Y.A., H.H., J.S.M., X.H., and B.B. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
NIH1R01DE023810
NIH1R01DE020102
NIH1R01DE026186
NIH Postdoctoral FellowshipF31DE026057
NIH1K99DE027719-01
NSF Graduate Research FellowshipDGE-1745303
Subject Keywords:Saccharibacteria; TM7; Actinomyces; Actinobacteria; periodontitis; candidate phyla radiation; bacterial symbiosis; human oral microbiome; human microbiome; inflammatory disease
Issue or Number:11
PubMed Central ID:PMC8595704
DOI:10.1016/j.chom.2021.09.009
Record Number:CaltechAUTHORS:20211022-170856506
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211022-170856506
Official Citation:Otari Chipashvili, Daniel R. Utter, Joseph K. Bedree, Yansong Ma, Fabian Schulte, Gabrielle Mascarin, Yasmin Alayyoubi, Deepak Chouhan, Markus Hardt, Felicitas Bidlack, Hatice Hasturk, Xuesong He, Jeffrey S. McLean, Batbileg Bor, Episymbiotic Saccharibacteria suppresses gingival inflammation and bone loss in mice through host bacterial modulation, Cell Host & Microbe, Volume 29, Issue 11, 2021, Pages 1649-1662.e7, ISSN 1931-3128, https://doi.org/10.1016/j.chom.2021.09.009. (https://www.sciencedirect.com/science/article/pii/S193131282100425X)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:111605
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Oct 2021 00:06
Last Modified:18 Nov 2021 22:51

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