The evolution and competitive strategies of Akkermansia muciniphila in gut

Akkermansia muciniphila is a commensal bacterium using mucin as its sole carbon and nitrogen source. A. muciniphila is a promising candidate for next-generation probiotics to prevent inflammatory and metabolic disorders, including diabetes and obesity, and to increase the response to cancer immunoth...

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Main Authors: Ji-Sun Kim, Se Won Kang, Ju Huck Lee, Seung-Hwan Park, Jung-Sook Lee
Format: Article
Language:English
Published: Taylor & Francis Group 2022-12-01
Series:Gut Microbes
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Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2021.2025017
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author Ji-Sun Kim
Se Won Kang
Ju Huck Lee
Seung-Hwan Park
Jung-Sook Lee
author_facet Ji-Sun Kim
Se Won Kang
Ju Huck Lee
Seung-Hwan Park
Jung-Sook Lee
author_sort Ji-Sun Kim
collection DOAJ
description Akkermansia muciniphila is a commensal bacterium using mucin as its sole carbon and nitrogen source. A. muciniphila is a promising candidate for next-generation probiotics to prevent inflammatory and metabolic disorders, including diabetes and obesity, and to increase the response to cancer immunotherapy. In this study, a comparative pan-genome analysis was conducted to investigate the genomic diversity and evolutionary relationships between complete genomes of 27 A. muciniphila strains, including KGMB strains isolated from healthy Koreans. The analysis showed that A. muciniphila strains formed two clades of group A and B in a phylogenetic tree constructed using 1,219 orthologous single-copy core genes. Interestingly, group A comprised of strains from human feces in Korea, whereas most of group B comprised strains from human feces in Europe and China, and from mouse feces. As group A and B branched, mucin hydrolysis played an important role in the stability of the core genome and drove evolution in the direction of defense against invading pathogens, survival in, and colonization in the mucus layer. In addition, WapA and anSME, which function in competition and post-translational modification of sulfatase, respectively, have been a particularly important selective pressure in the evolution of group A. KGMB strains in group A with anSME gene showed sulfatase activity, but KCTC 15667T in group B without anSME did not. Our findings revealed that KGMB strains evolved to gain an edge in the competition with other gut bacteria by increasing the utilization of sulfated mucin, which will allow it to become highly colonized in the gut environment.
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spelling doaj-art-3b01bbd6756c4e8ea2e085c85b00afc12025-08-20T03:21:40ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2021.2025017The evolution and competitive strategies of Akkermansia muciniphila in gutJi-Sun Kim0Se Won Kang1Ju Huck Lee2Seung-Hwan Park3Jung-Sook Lee4Korean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology, Jeongeup-si, Republic of KoreaKorean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology, Jeongeup-si, Republic of KoreaKorean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology, Jeongeup-si, Republic of KoreaKorean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology, Jeongeup-si, Republic of KoreaKorean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology, Jeongeup-si, Republic of KoreaAkkermansia muciniphila is a commensal bacterium using mucin as its sole carbon and nitrogen source. A. muciniphila is a promising candidate for next-generation probiotics to prevent inflammatory and metabolic disorders, including diabetes and obesity, and to increase the response to cancer immunotherapy. In this study, a comparative pan-genome analysis was conducted to investigate the genomic diversity and evolutionary relationships between complete genomes of 27 A. muciniphila strains, including KGMB strains isolated from healthy Koreans. The analysis showed that A. muciniphila strains formed two clades of group A and B in a phylogenetic tree constructed using 1,219 orthologous single-copy core genes. Interestingly, group A comprised of strains from human feces in Korea, whereas most of group B comprised strains from human feces in Europe and China, and from mouse feces. As group A and B branched, mucin hydrolysis played an important role in the stability of the core genome and drove evolution in the direction of defense against invading pathogens, survival in, and colonization in the mucus layer. In addition, WapA and anSME, which function in competition and post-translational modification of sulfatase, respectively, have been a particularly important selective pressure in the evolution of group A. KGMB strains in group A with anSME gene showed sulfatase activity, but KCTC 15667T in group B without anSME did not. Our findings revealed that KGMB strains evolved to gain an edge in the competition with other gut bacteria by increasing the utilization of sulfated mucin, which will allow it to become highly colonized in the gut environment.https://www.tandfonline.com/doi/10.1080/19490976.2021.2025017Akkermansia muciniphilaevolutionenvironmental adaptationcomparative genomic analysis
spellingShingle Ji-Sun Kim
Se Won Kang
Ju Huck Lee
Seung-Hwan Park
Jung-Sook Lee
The evolution and competitive strategies of Akkermansia muciniphila in gut
Gut Microbes
Akkermansia muciniphila
evolution
environmental adaptation
comparative genomic analysis
title The evolution and competitive strategies of Akkermansia muciniphila in gut
title_full The evolution and competitive strategies of Akkermansia muciniphila in gut
title_fullStr The evolution and competitive strategies of Akkermansia muciniphila in gut
title_full_unstemmed The evolution and competitive strategies of Akkermansia muciniphila in gut
title_short The evolution and competitive strategies of Akkermansia muciniphila in gut
title_sort evolution and competitive strategies of akkermansia muciniphila in gut
topic Akkermansia muciniphila
evolution
environmental adaptation
comparative genomic analysis
url https://www.tandfonline.com/doi/10.1080/19490976.2021.2025017
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