Mobile genes in the human microbiome are structured from global to individual scales

Recent work has underscored the importance of the microbiome in human health, and has largely attributed differences in phenotype to differences in the species present among individuals. However, mobile genes can confer profoundly different phenotypes on different strains of the same species. Little...

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Main Authors: Yilmaz, S., Huang, K., Xu, L., Jupiter, S. D., Jenkins, A. P., Naisilisili, W., Tamminen, M., Wortman, J. R., Birren, B. W., Blainey, P. C., Singh, A. K., Gevers, D., Brito, Ilana Lauren, Smillie, Chris S, Alm, Eric J, Xavier, Ramnik Joseph
Other Authors: Institute for Medical Engineering and Science
Format: Article
Language:en_US
Published: Nature Publishing Group 2017
Online Access:http://hdl.handle.net/1721.1/106826
https://orcid.org/0000-0002-8202-5222
https://orcid.org/0000-0001-8294-9364
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author Yilmaz, S.
Huang, K.
Xu, L.
Jupiter, S. D.
Jenkins, A. P.
Naisilisili, W.
Tamminen, M.
Wortman, J. R.
Birren, B. W.
Blainey, P. C.
Singh, A. K.
Gevers, D.
Brito, Ilana Lauren
Smillie, Chris S
Alm, Eric J
Xavier, Ramnik Joseph
author2 Institute for Medical Engineering and Science
author_facet Institute for Medical Engineering and Science
Yilmaz, S.
Huang, K.
Xu, L.
Jupiter, S. D.
Jenkins, A. P.
Naisilisili, W.
Tamminen, M.
Wortman, J. R.
Birren, B. W.
Blainey, P. C.
Singh, A. K.
Gevers, D.
Brito, Ilana Lauren
Smillie, Chris S
Alm, Eric J
Xavier, Ramnik Joseph
author_sort Yilmaz, S.
collection MIT
description Recent work has underscored the importance of the microbiome in human health, and has largely attributed differences in phenotype to differences in the species present among individuals. However, mobile genes can confer profoundly different phenotypes on different strains of the same species. Little is known about the function and distribution of mobile genes in the human microbiome, and in particular whether the gene pool is globally homogenous or constrained by human population structure. Here, we investigate this question by comparing the mobile genes found in the microbiomes of 81 metropolitan North Americans with those of 172 agrarian Fiji islanders using a combination of single-cell genomics and metagenomics. We find large differences in mobile gene content between the Fijian and North American microbiomes, with functional variation that mirrors known dietary differences such as the excess of plant-based starch degradation genes found in Fijian individuals. Notably, we also observed differences between the mobile gene pools of neighbouring Fijian villages, even though microbiome composition across villages is similar. Finally, we observe high rates of recombination leading to individual-specific mobile elements, suggesting that the abundance of some genes may reflect environmental selection rather than dispersal limitation. Together, these data support the hypothesis that human activities and behaviours provide selective pressures that shape mobile gene pools, and that acquisition of mobile genes is important for colonizing specific human populations.
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spelling mit-1721.1/1068262022-09-30T20:36:51Z Mobile genes in the human microbiome are structured from global to individual scales Yilmaz, S. Huang, K. Xu, L. Jupiter, S. D. Jenkins, A. P. Naisilisili, W. Tamminen, M. Wortman, J. R. Birren, B. W. Blainey, P. C. Singh, A. K. Gevers, D. Brito, Ilana Lauren Smillie, Chris S Alm, Eric J Xavier, Ramnik Joseph Institute for Medical Engineering and Science Massachusetts Institute of Technology. Department of Biological Engineering Brito, Ilana Lauren Smillie, Chris S Alm, Eric J Xavier, Ramnik Joseph Recent work has underscored the importance of the microbiome in human health, and has largely attributed differences in phenotype to differences in the species present among individuals. However, mobile genes can confer profoundly different phenotypes on different strains of the same species. Little is known about the function and distribution of mobile genes in the human microbiome, and in particular whether the gene pool is globally homogenous or constrained by human population structure. Here, we investigate this question by comparing the mobile genes found in the microbiomes of 81 metropolitan North Americans with those of 172 agrarian Fiji islanders using a combination of single-cell genomics and metagenomics. We find large differences in mobile gene content between the Fijian and North American microbiomes, with functional variation that mirrors known dietary differences such as the excess of plant-based starch degradation genes found in Fijian individuals. Notably, we also observed differences between the mobile gene pools of neighbouring Fijian villages, even though microbiome composition across villages is similar. Finally, we observe high rates of recombination leading to individual-specific mobile elements, suggesting that the abundance of some genes may reflect environmental selection rather than dispersal limitation. Together, these data support the hypothesis that human activities and behaviours provide selective pressures that shape mobile gene pools, and that acquisition of mobile genes is important for colonizing specific human populations. National Human Genome Research Institute (U.S.) (Grant U54HG003067) Broad Institute of MIT and Harvard Massachusetts Institute of Technology. Center for Environmental Health Sciences Massachusetts Institute of Technology. Center for Microbiome Informatics and Therapeutics Fiji. Ministry of Health Columbia Earth Institute (Institute Fellowship) 2017-02-02T18:07:28Z 2017-02-02T18:07:28Z 2016-07 2015-02 Article http://purl.org/eprint/type/JournalArticle 0028-0836 1476-4687 http://hdl.handle.net/1721.1/106826 Brito, I. L. et al. “Mobile Genes in the Human Microbiome Are Structured from Global to Individual Scales.” Nature 535.7612 (2016): 435–439. https://orcid.org/0000-0002-8202-5222 https://orcid.org/0000-0001-8294-9364 en_US http://dx.doi.org/10.1038/nature18927 Nature Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Nature Publishing Group PMC
spellingShingle Yilmaz, S.
Huang, K.
Xu, L.
Jupiter, S. D.
Jenkins, A. P.
Naisilisili, W.
Tamminen, M.
Wortman, J. R.
Birren, B. W.
Blainey, P. C.
Singh, A. K.
Gevers, D.
Brito, Ilana Lauren
Smillie, Chris S
Alm, Eric J
Xavier, Ramnik Joseph
Mobile genes in the human microbiome are structured from global to individual scales
title Mobile genes in the human microbiome are structured from global to individual scales
title_full Mobile genes in the human microbiome are structured from global to individual scales
title_fullStr Mobile genes in the human microbiome are structured from global to individual scales
title_full_unstemmed Mobile genes in the human microbiome are structured from global to individual scales
title_short Mobile genes in the human microbiome are structured from global to individual scales
title_sort mobile genes in the human microbiome are structured from global to individual scales
url http://hdl.handle.net/1721.1/106826
https://orcid.org/0000-0002-8202-5222
https://orcid.org/0000-0001-8294-9364
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