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Genome-Centric Dynamics Shape the Diversity of Oral Bacterial Populations

Utter, Daniel R. and Cavanaugh, Colleen M. and Borisy, Gary G. (2022) Genome-Centric Dynamics Shape the Diversity of Oral Bacterial Populations. mBio, 13 (6). pp. 2414-2422. ISSN 2150-7511. doi:10.1128/mbio.02414-22.

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Two major viewpoints have been put forward for how microbial populations change, differing in whether adaptation is driven principally by gene-centric or genome-centric processes. Longitudinal sampling at microbially relevant timescales, i.e., days to weeks, is critical for distinguishing these mechanisms. Because of its significance for both microbial ecology and human health and its accessibility and high level of curation, we used the oral microbiota to study bacterial intrapopulation genome dynamics. Metagenomes were generated by shotgun sequencing of total community DNA from the healthy tongues of 17 volunteers at four to seven time points obtained over intervals of days to weeks. We obtained 390 high-quality metagenome-assembled genomes (MAGs) defining population genomes from 55 genera. The vast majority of genes in each MAG were tightly linked over the 2-week sampling window, indicating that the majority of the population’s genomes were temporally stable at the MAG level. MAG-defined populations were composed of up to 5 strains, as determined by single-nucleotide-variant frequencies. Although most were stable over time, individual strains carrying over 100 distinct genes that rose from low abundance to dominance in a population over a period of days were detected. These results indicate a genome-wide as opposed to a gene-level process of population change. We infer that genome-wide selection of ecotypes is the dominant mode of adaptation in the oral populations over short timescales.

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Utter, Daniel R.0000-0003-3322-7108
Cavanaugh, Colleen M.0000-0002-1114-9084
Additional Information:We thank Otto X. Cordero and I-Ting Huang for helpful discussions. We thank the many volunteers who donated samples. The content is solely those of the authors and does not necessarily reflect the views of Harvard Catalyst, Harvard University and its affiliated academic health care centers, the National Science Foundation, or the National Institutes of Health. We declare that we have no competing interests. Support was provided to D.R.U., C.M.C., and G.G.B. from Harvard Catalyst, The Harvard Clinical and Translational Science Center (National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health Award UL1 TR001102 and financial contributions from Harvard University and its affiliated academic health care centers). Additional support was provided from NIH grant DE022586 to G.G.B. Additional support was provided by the National Science Foundation Graduate Research Fellowship Program under grant DGE1745303 to D.R.U. Additional support was provided to D.R.U. by Harvard University’s Department of Organismic and Evolutionary Biology Program. D.R.U., C.M.C., and G.G.B. designed research; D.R.U., C.M.C., and G.G.B. performed research and analyzed data; D.R.U., C.M.C., and G.G.B. wrote the paper.
Funding AgencyGrant Number
NIHUL1 TR001102
NSF Graduate Research FellowshipDGE-1745303
Harvard UniversityUNSPECIFIED
Issue or Number:6
Record Number:CaltechAUTHORS:20221020-736967400.11
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:117511
Deposited By: Research Services Depository
Deposited On:28 Oct 2022 15:21
Last Modified:25 Jan 2023 19:04

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