Lifestyle and Horizontal Gene Transfer-Mediated Evolution of <named-content content-type="genus-species">Mucispirillum schaedleri</named-content>, a Core Member of the Murine Gut Microbiota

ABSTRACT Mucispirillum schaedleri is an abundant inhabitant of the intestinal mucus layer of rodents and other animals and has been suggested to be a pathobiont, a commensal that plays a role in disease. In order to gain insights into its lifestyle, we analyzed the genome and transcriptome of M. sch...

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Autores principales: Alexander Loy, Carina Pfann, Michaela Steinberger, Buck Hanson, Simone Herp, Sandrine Brugiroux, João Carlos Gomes Neto, Mark V. Boekschoten, Clarissa Schwab, Tim Urich, Amanda E. Ramer-Tait, Thomas Rattei, Bärbel Stecher, David Berry
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:3a027c7682614c98bc892019f48270a62021-12-02T19:48:49ZLifestyle and Horizontal Gene Transfer-Mediated Evolution of <named-content content-type="genus-species">Mucispirillum schaedleri</named-content>, a Core Member of the Murine Gut Microbiota10.1128/mSystems.00171-162379-5077https://doaj.org/article/3a027c7682614c98bc892019f48270a62017-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00171-16https://doaj.org/toc/2379-5077ABSTRACT Mucispirillum schaedleri is an abundant inhabitant of the intestinal mucus layer of rodents and other animals and has been suggested to be a pathobiont, a commensal that plays a role in disease. In order to gain insights into its lifestyle, we analyzed the genome and transcriptome of M. schaedleri ASF 457 and performed physiological experiments to test traits predicted by its genome. Although described as a mucus inhabitant, M. schaedleri has limited capacity for degrading host-derived mucosal glycans and other complex polysaccharides. Additionally, M. schaedleri reduces nitrate and expresses systems for scavenging oxygen and reactive oxygen species in vivo, which may account for its localization close to the mucosal tissue and expansion during inflammation. Also of note, M. schaedleri harbors a type VI secretion system and putative effector proteins and can modify gene expression in mucosal tissue, suggesting intimate interactions with its host and a possible role in inflammation. The M. schaedleri genome has been shaped by extensive horizontal gene transfer, primarily from intestinal Epsilon- and Deltaproteobacteria, indicating that horizontal gene transfer has played a key role in defining its niche in the gut ecosystem. IMPORTANCE Shifts in gut microbiota composition have been associated with intestinal inflammation, but it remains unclear whether inflammation-associated bacteria are commensal or detrimental to their host. Here, we studied the lifestyle of the gut bacterium Mucispirillum schaedleri, which is associated with inflammation in widely used mouse models. We found that M. schaedleri has specialized systems to handle oxidative stress during inflammation. Additionally, it expresses secretion systems and effector proteins and can modify the mucosal gene expression of its host. This suggests that M. schaedleri undergoes intimate interactions with its host and may play a role in inflammation. The insights presented here aid our understanding of how commensal gut bacteria may be involved in altering susceptibility to disease.Alexander LoyCarina PfannMichaela SteinbergerBuck HansonSimone HerpSandrine BrugirouxJoão Carlos Gomes NetoMark V. BoekschotenClarissa SchwabTim UrichAmanda E. Ramer-TaitThomas RatteiBärbel StecherDavid BerryAmerican Society for MicrobiologyarticleDNRADeferribacteresgut microbiotaHelicobacterfluorescence in situ hybridizationmetatranscriptomicsMicrobiologyQR1-502ENmSystems, Vol 2, Iss 1 (2017)
institution DOAJ
collection DOAJ
language EN
topic DNRA
Deferribacteres
gut microbiota
Helicobacter
fluorescence in situ hybridization
metatranscriptomics
Microbiology
QR1-502
spellingShingle DNRA
Deferribacteres
gut microbiota
Helicobacter
fluorescence in situ hybridization
metatranscriptomics
Microbiology
QR1-502
Alexander Loy
Carina Pfann
Michaela Steinberger
Buck Hanson
Simone Herp
Sandrine Brugiroux
João Carlos Gomes Neto
Mark V. Boekschoten
Clarissa Schwab
Tim Urich
Amanda E. Ramer-Tait
Thomas Rattei
Bärbel Stecher
David Berry
Lifestyle and Horizontal Gene Transfer-Mediated Evolution of <named-content content-type="genus-species">Mucispirillum schaedleri</named-content>, a Core Member of the Murine Gut Microbiota
description ABSTRACT Mucispirillum schaedleri is an abundant inhabitant of the intestinal mucus layer of rodents and other animals and has been suggested to be a pathobiont, a commensal that plays a role in disease. In order to gain insights into its lifestyle, we analyzed the genome and transcriptome of M. schaedleri ASF 457 and performed physiological experiments to test traits predicted by its genome. Although described as a mucus inhabitant, M. schaedleri has limited capacity for degrading host-derived mucosal glycans and other complex polysaccharides. Additionally, M. schaedleri reduces nitrate and expresses systems for scavenging oxygen and reactive oxygen species in vivo, which may account for its localization close to the mucosal tissue and expansion during inflammation. Also of note, M. schaedleri harbors a type VI secretion system and putative effector proteins and can modify gene expression in mucosal tissue, suggesting intimate interactions with its host and a possible role in inflammation. The M. schaedleri genome has been shaped by extensive horizontal gene transfer, primarily from intestinal Epsilon- and Deltaproteobacteria, indicating that horizontal gene transfer has played a key role in defining its niche in the gut ecosystem. IMPORTANCE Shifts in gut microbiota composition have been associated with intestinal inflammation, but it remains unclear whether inflammation-associated bacteria are commensal or detrimental to their host. Here, we studied the lifestyle of the gut bacterium Mucispirillum schaedleri, which is associated with inflammation in widely used mouse models. We found that M. schaedleri has specialized systems to handle oxidative stress during inflammation. Additionally, it expresses secretion systems and effector proteins and can modify the mucosal gene expression of its host. This suggests that M. schaedleri undergoes intimate interactions with its host and may play a role in inflammation. The insights presented here aid our understanding of how commensal gut bacteria may be involved in altering susceptibility to disease.
format article
author Alexander Loy
Carina Pfann
Michaela Steinberger
Buck Hanson
Simone Herp
Sandrine Brugiroux
João Carlos Gomes Neto
Mark V. Boekschoten
Clarissa Schwab
Tim Urich
Amanda E. Ramer-Tait
Thomas Rattei
Bärbel Stecher
David Berry
author_facet Alexander Loy
Carina Pfann
Michaela Steinberger
Buck Hanson
Simone Herp
Sandrine Brugiroux
João Carlos Gomes Neto
Mark V. Boekschoten
Clarissa Schwab
Tim Urich
Amanda E. Ramer-Tait
Thomas Rattei
Bärbel Stecher
David Berry
author_sort Alexander Loy
title Lifestyle and Horizontal Gene Transfer-Mediated Evolution of <named-content content-type="genus-species">Mucispirillum schaedleri</named-content>, a Core Member of the Murine Gut Microbiota
title_short Lifestyle and Horizontal Gene Transfer-Mediated Evolution of <named-content content-type="genus-species">Mucispirillum schaedleri</named-content>, a Core Member of the Murine Gut Microbiota
title_full Lifestyle and Horizontal Gene Transfer-Mediated Evolution of <named-content content-type="genus-species">Mucispirillum schaedleri</named-content>, a Core Member of the Murine Gut Microbiota
title_fullStr Lifestyle and Horizontal Gene Transfer-Mediated Evolution of <named-content content-type="genus-species">Mucispirillum schaedleri</named-content>, a Core Member of the Murine Gut Microbiota
title_full_unstemmed Lifestyle and Horizontal Gene Transfer-Mediated Evolution of <named-content content-type="genus-species">Mucispirillum schaedleri</named-content>, a Core Member of the Murine Gut Microbiota
title_sort lifestyle and horizontal gene transfer-mediated evolution of <named-content content-type="genus-species">mucispirillum schaedleri</named-content>, a core member of the murine gut microbiota
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/3a027c7682614c98bc892019f48270a6
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