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Genomic adaptations of Campylobacter jejuni to long-term human colonization

BACKGROUND: Campylobacter is a genus of bacteria that has been isolated from the gastrointestinal tract of humans and animals, and the environments they inhabit around the world. Campylobacter adapt to new environments by changes in their gene content and expression, but little is known about how th...

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Autores principales: Bloomfield, Samuel J., Midwinter, Anne C., Biggs, Patrick J., French, Nigel P., Marshall, Jonathan C., Hayman, David T. S., Carter, Philip E., Mather, Alison E., Fayaz, Ahmed, Thornley, Craig, Kelly, David J., Benschop, Jackie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8665580/
https://www.ncbi.nlm.nih.gov/pubmed/34893079
http://dx.doi.org/10.1186/s13099-021-00469-7
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author Bloomfield, Samuel J.
Midwinter, Anne C.
Biggs, Patrick J.
French, Nigel P.
Marshall, Jonathan C.
Hayman, David T. S.
Carter, Philip E.
Mather, Alison E.
Fayaz, Ahmed
Thornley, Craig
Kelly, David J.
Benschop, Jackie
author_facet Bloomfield, Samuel J.
Midwinter, Anne C.
Biggs, Patrick J.
French, Nigel P.
Marshall, Jonathan C.
Hayman, David T. S.
Carter, Philip E.
Mather, Alison E.
Fayaz, Ahmed
Thornley, Craig
Kelly, David J.
Benschop, Jackie
author_sort Bloomfield, Samuel J.
collection PubMed
description BACKGROUND: Campylobacter is a genus of bacteria that has been isolated from the gastrointestinal tract of humans and animals, and the environments they inhabit around the world. Campylobacter adapt to new environments by changes in their gene content and expression, but little is known about how they adapt to long-term human colonization. In this study, the genomes of 31 isolates from a New Zealand patient and 22 isolates from a United Kingdom patient belonging to Campylobacter jejuni sequence type 45 (ST45) were compared with 209 ST45 genomes from other sources to identify the mechanisms by which Campylobacter adapts to long-term human colonization. In addition, the New Zealand patient had their microbiota investigated using 16S rRNA metabarcoding, and their level of inflammation and immunosuppression analyzed using biochemical tests, to determine how Campylobacter adapts to a changing gastrointestinal tract. RESULTS: There was some evidence that long-term colonization led to genome degradation, but more evidence that Campylobacter adapted through the accumulation of non-synonymous single nucleotide polymorphisms (SNPs) and frameshifts in genes involved in cell motility, signal transduction and the major outer membrane protein (MOMP). The New Zealand patient also displayed considerable variation in their microbiome, inflammation and immunosuppression over five months, and the Campylobacter collected from this patient could be divided into two subpopulations, the proportion of which correlated with the amount of gastrointestinal inflammation. CONCLUSIONS: This study demonstrates how genomics, phylogenetics, 16S rRNA metabarcoding and biochemical markers can provide insight into how Campylobacter adapts to changing environments within human hosts. This study also demonstrates that long-term human colonization selects for changes in Campylobacter genes involved in cell motility, signal transduction and the MOMP; and that genetically distinct subpopulations of Campylobacter evolve to adapt to the changing gastrointestinal environment. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13099-021-00469-7.
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spelling pubmed-86655802021-12-13 Genomic adaptations of Campylobacter jejuni to long-term human colonization Bloomfield, Samuel J. Midwinter, Anne C. Biggs, Patrick J. French, Nigel P. Marshall, Jonathan C. Hayman, David T. S. Carter, Philip E. Mather, Alison E. Fayaz, Ahmed Thornley, Craig Kelly, David J. Benschop, Jackie Gut Pathog Research BACKGROUND: Campylobacter is a genus of bacteria that has been isolated from the gastrointestinal tract of humans and animals, and the environments they inhabit around the world. Campylobacter adapt to new environments by changes in their gene content and expression, but little is known about how they adapt to long-term human colonization. In this study, the genomes of 31 isolates from a New Zealand patient and 22 isolates from a United Kingdom patient belonging to Campylobacter jejuni sequence type 45 (ST45) were compared with 209 ST45 genomes from other sources to identify the mechanisms by which Campylobacter adapts to long-term human colonization. In addition, the New Zealand patient had their microbiota investigated using 16S rRNA metabarcoding, and their level of inflammation and immunosuppression analyzed using biochemical tests, to determine how Campylobacter adapts to a changing gastrointestinal tract. RESULTS: There was some evidence that long-term colonization led to genome degradation, but more evidence that Campylobacter adapted through the accumulation of non-synonymous single nucleotide polymorphisms (SNPs) and frameshifts in genes involved in cell motility, signal transduction and the major outer membrane protein (MOMP). The New Zealand patient also displayed considerable variation in their microbiome, inflammation and immunosuppression over five months, and the Campylobacter collected from this patient could be divided into two subpopulations, the proportion of which correlated with the amount of gastrointestinal inflammation. CONCLUSIONS: This study demonstrates how genomics, phylogenetics, 16S rRNA metabarcoding and biochemical markers can provide insight into how Campylobacter adapts to changing environments within human hosts. This study also demonstrates that long-term human colonization selects for changes in Campylobacter genes involved in cell motility, signal transduction and the MOMP; and that genetically distinct subpopulations of Campylobacter evolve to adapt to the changing gastrointestinal environment. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13099-021-00469-7. BioMed Central 2021-12-10 /pmc/articles/PMC8665580/ /pubmed/34893079 http://dx.doi.org/10.1186/s13099-021-00469-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Bloomfield, Samuel J.
Midwinter, Anne C.
Biggs, Patrick J.
French, Nigel P.
Marshall, Jonathan C.
Hayman, David T. S.
Carter, Philip E.
Mather, Alison E.
Fayaz, Ahmed
Thornley, Craig
Kelly, David J.
Benschop, Jackie
Genomic adaptations of Campylobacter jejuni to long-term human colonization
title Genomic adaptations of Campylobacter jejuni to long-term human colonization
title_full Genomic adaptations of Campylobacter jejuni to long-term human colonization
title_fullStr Genomic adaptations of Campylobacter jejuni to long-term human colonization
title_full_unstemmed Genomic adaptations of Campylobacter jejuni to long-term human colonization
title_short Genomic adaptations of Campylobacter jejuni to long-term human colonization
title_sort genomic adaptations of campylobacter jejuni to long-term human colonization
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8665580/
https://www.ncbi.nlm.nih.gov/pubmed/34893079
http://dx.doi.org/10.1186/s13099-021-00469-7
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