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Acquisition of the arginine deiminase system benefits epiparasitic Saccharibacteria and their host bacteria in a mammalian niche environment

Tian, Jing and Utter, Daniel R. and Cen, Lujia and Dong, Pu-Ting and Shi, Wenyuan and Bor, Batbileg and Qin, Man and McLean, Jeffrey S. and He, Xuesong (2022) Acquisition of the arginine deiminase system benefits epiparasitic Saccharibacteria and their host bacteria in a mammalian niche environment. Proceedings of the National Academy of Sciences of the United States of America, 119 (2). Art. No. e2114909119. ISSN 0027-8424. PMCID PMC8764695. doi:10.1073/pnas.2114909119. https://resolver.caltech.edu/CaltechAUTHORS:20220110-745200400

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Abstract

Saccharibacteria are a group of widespread and genetically diverse ultrasmall bacteria with highly reduced genomes that belong to the Candidate Phyla Radiation. Comparative genomic analyses suggest convergent evolution of key functions enabling the adaptation of environmental Saccharibacteria to mammalian microbiomes. Currently, our understanding of this environment-to-mammal niche transition within Saccharibacteria and their obligate episymbiotic association with host bacteria is limited. Here, we identified a complete arginine deiminase system (ADS), found in further genome streamlined mammal-associated Saccharibacteria but missing in their environmental counterparts, suggesting acquisition during environment-to-mammal niche transition. Using TM7x, the first cultured Saccharibacteria strain from the human oral microbiome and its host bacterium Actinomyces odontolyticus, we experimentally tested the function and impact of the ADS. We demonstrated that by catabolizing arginine and generating adenosine triphosphate, the ADS allows metabolically restrained TM7x to maintain higher viability and infectivity when disassociated from the host bacterium. Furthermore, the ADS protects TM7x and its host bacterium from acid stress, a condition frequently encountered within the human oral cavity due to bacterial metabolism of dietary carbohydrates. Intriguingly, with a restricted host range, TM7x forms obligate associations with Actinomyces spp. lacking the ADS but not those carrying the ADS, suggesting the acquired ADS may also contribute to partner selection for cooperative episymbiosis within a mammalian microbiome. These data present experimental characterization of a mutualistic interaction between TM7x and their host bacteria, and illustrate the benefits of acquiring a novel pathway in the transition of Saccharibacteria to mammalian microbiomes.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.2114909119DOIArticle
https://www.pnas.org/content/suppl/2022/01/06/2114909119.DCSupplementalPublisherSupporting Information
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc8764695/PubMed CentralArticle
ORCID:
AuthorORCID
Tian, Jing0000-0003-2276-9286
Utter, Daniel R.0000-0003-3322-7108
McLean, Jeffrey S.0000-0001-9934-5137
He, Xuesong0000-0002-3333-9188
Additional Information:© 2022 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Edited by Edward DeLong, Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaii at Manoa, Honolulu, HI; received August 12, 2021; accepted November 19, 2021. We thank Dr. Felicitas Bidlack and Dr. Pallavi Murugkar at The Forsyth Institute for assisting with acquisition of scanning electron microscopy images. We thank Dr. Fabian Schulte at Brandeis University for insightful discussions. Research in this publication was supported by the National Institute of Dental and Craniofacial Research of the NIH under Awards 1R01DE023810, 1R01DE020102, and 1R01DE026186 (to X.H., J.S.M., and W.S.) and F32DE025548-01 and 1K99DE027719-01 (to B.B.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Data Availability: All study data are included in the article and/or SI Appendix. Author contributions: J.T. and X.H. designed research; J.T., L.C., P.-T.D., and X.H. performed research; J.T., D.R.U., W.S., B.B., M.Q., J.S.M., and X.H. analyzed data; and J.T., D.R.U., W.S., B.B., M.Q., J.S.M., and X.H. wrote the paper. The authors declare no competing interest. This article is a PNAS Direct Submission. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2114909119/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NIH1R01DE023810
NIH1R01DE020102
NIH1R01DE026186
NIH Postdoctoral FellowshipF32DE025548-01
NIH1K99DE027719-01
Subject Keywords:Saccharibacteria; episymbiosis; arginine deiminase system; oral microbiome; TM7
Issue or Number:2
PubMed Central ID:PMC8764695
DOI:10.1073/pnas.2114909119
Record Number:CaltechAUTHORS:20220110-745200400
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220110-745200400
Official Citation:Acquisition of the arginine deiminase system benefits epiparasitic Saccharibacteria and their host bacteria in a mammalian niche environment. Jing Tian, Daniel R. Utter, Lujia Cen, Pu-Ting Dong, Wenyuan Shi, Batbileg Bor, Man Qin, Jeffrey S. McLean, Xuesong He. Proceedings of the National Academy of Sciences Jan 2022, 119 (2) e2114909119; DOI: 10.1073/pnas.2114909119
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:112805
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:10 Jan 2022 16:56
Last Modified:28 Jan 2022 19:33

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