A cryptic plasmid is among the most numerous genetic elements in the human gut

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Date
2024-02-29
Authors
Fogarty, Emily C.
Schechter, Matthew S.
Lolans, Karen
Sheahan, Madeline L.
Veseli, Iva A.
Moore, Ryan M.
Kiefl, Evan
Moody, Thomas
Rice, Phoebe A.
Yu, Michael K.
Mimee, Mark
Chang, Eugene B.
Ruscheweyh, Hans-Joachim
Sunagawa, Shinichi
McLellan, Sandra L.
Willis, Amy D.
Comstock, Laurie E.
Eren, A. Murat
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10.1016/j.cell.2024.01.039
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Keywords
Plasmid
Cryptic
Metagenomics
Horizontal gene transfer
Mobile genetic element
Inflammatory bowel disease
Bacteroides
Sewage
Human gut microbiome
Abstract
Plasmids are extrachromosomal genetic elements that often encode fitness-enhancing features. However, many bacteria carry “cryptic” plasmids that do not confer clear beneficial functions. We identified one such cryptic plasmid, pBI143, which is ubiquitous across industrialized gut microbiomes and is 14 times as numerous as crAssphage, currently established as the most abundant extrachromosomal genetic element in the human gut. The majority of mutations in pBI143 accumulate in specific positions across thousands of metagenomes, indicating strong purifying selection. pBI143 is monoclonal in most individuals, likely due to the priority effect of the version first acquired, often from one’s mother. pBI143 can transfer between Bacteroidales, and although it does not appear to impact bacterial host fitness in vivo, it can transiently acquire additional genetic content. We identified important practical applications of pBI143, including its use in identifying human fecal contamination and its potential as an alternative approach to track human colonic inflammatory states.
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© The Author(s), 2024. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Fogarty, E. C., Schechter, M. S., Lolans, K., Sheahan, M. L., Veseli, I., Moore, R. M., Kiefl, E., Moody, T., Rice, P. A., Yu, M. K., Mimee, M., Chang, E. B., Ruscheweyh, H.-J., Sunagawa, S., Mclellan, S. L., Willis, A. D., Comstock, L. E., & Eren, A. M. (2024). A cryptic plasmid is among the most numerous genetic elements in the human gut. Cell, 187(5), 1206-1222.e16, https://doi.org/10.1016/j.cell.2024.01.039.
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Fogarty, E. C., Schechter, M. S., Lolans, K., Sheahan, M. L., Veseli, I., Moore, R. M., Kiefl, E., Moody, T., Rice, P. A., Yu, M. K., Mimee, M., Chang, E. B., Ruscheweyh, H.-J., Sunagawa, S., Mclellan, S. L., Willis, A. D., Comstock, L. E., & Eren, A. M. (2024). A cryptic plasmid is among the most numerous genetic elements in the human gut. Cell, 187(5), 1206-1222.e16.
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