Cargando…
Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability
Campylobacter jejuni, the most frequent cause of food‐borne bacterial gastroenteritis worldwide, is a microaerophile that has to survive high environmental oxygen tensions, adapt to oxygen limitation in the intestine and resist host oxidative attack. Here, oxygen‐dependent changes in C. jejuni physi...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2017
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5656828/ https://www.ncbi.nlm.nih.gov/pubmed/28892295 http://dx.doi.org/10.1111/1462-2920.13930 |
_version_ | 1783273773794852864 |
---|---|
author | Guccione, Edward J. Kendall, John J. Hitchcock, Andrew Garg, Nitanshu White, Michael A. Mulholland, Francis Poole, Robert K. Kelly, David J. |
author_facet | Guccione, Edward J. Kendall, John J. Hitchcock, Andrew Garg, Nitanshu White, Michael A. Mulholland, Francis Poole, Robert K. Kelly, David J. |
author_sort | Guccione, Edward J. |
collection | PubMed |
description | Campylobacter jejuni, the most frequent cause of food‐borne bacterial gastroenteritis worldwide, is a microaerophile that has to survive high environmental oxygen tensions, adapt to oxygen limitation in the intestine and resist host oxidative attack. Here, oxygen‐dependent changes in C. jejuni physiology were studied at constant growth rate using carbon (serine)‐limited continuous chemostat cultures. We show that a perceived aerobiosis scale can be calibrated by the acetate excretion flux, which becomes zero when metabolism is fully aerobic (100% aerobiosis). Transcriptome changes in a downshift experiment from 150% to 40% aerobiosis revealed many novel oxygen‐regulated genes and highlighted re‐modelling of the electron transport chains. A label‐free proteomic analysis showed that at 40% aerobiosis, many proteins involved in host colonisation (e.g., PorA, CadF, FlpA, CjkT) became more abundant. PorA abundance increased steeply below 100% aerobiosis. In contrast, several citric‐acid cycle enzymes, the peptide transporter CstA, PEB1 aspartate/glutamate transporter, LutABC lactate dehydrogenase and PutA proline dehydrogenase became more abundant with increasing aerobiosis. We also observed a co‐ordinated response of oxidative stress protection enzymes and Fe‐S cluster biogenesis proteins above 100% aerobiosis. Our approaches reveal key virulence factors that respond to restricted oxygen availability and specific transporters and catabolic pathways activated with increasing aerobiosis. |
format | Online Article Text |
id | pubmed-5656828 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-56568282017-11-01 Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability Guccione, Edward J. Kendall, John J. Hitchcock, Andrew Garg, Nitanshu White, Michael A. Mulholland, Francis Poole, Robert K. Kelly, David J. Environ Microbiol Research Articles Campylobacter jejuni, the most frequent cause of food‐borne bacterial gastroenteritis worldwide, is a microaerophile that has to survive high environmental oxygen tensions, adapt to oxygen limitation in the intestine and resist host oxidative attack. Here, oxygen‐dependent changes in C. jejuni physiology were studied at constant growth rate using carbon (serine)‐limited continuous chemostat cultures. We show that a perceived aerobiosis scale can be calibrated by the acetate excretion flux, which becomes zero when metabolism is fully aerobic (100% aerobiosis). Transcriptome changes in a downshift experiment from 150% to 40% aerobiosis revealed many novel oxygen‐regulated genes and highlighted re‐modelling of the electron transport chains. A label‐free proteomic analysis showed that at 40% aerobiosis, many proteins involved in host colonisation (e.g., PorA, CadF, FlpA, CjkT) became more abundant. PorA abundance increased steeply below 100% aerobiosis. In contrast, several citric‐acid cycle enzymes, the peptide transporter CstA, PEB1 aspartate/glutamate transporter, LutABC lactate dehydrogenase and PutA proline dehydrogenase became more abundant with increasing aerobiosis. We also observed a co‐ordinated response of oxidative stress protection enzymes and Fe‐S cluster biogenesis proteins above 100% aerobiosis. Our approaches reveal key virulence factors that respond to restricted oxygen availability and specific transporters and catabolic pathways activated with increasing aerobiosis. John Wiley and Sons Inc. 2017-10-02 2017-10 /pmc/articles/PMC5656828/ /pubmed/28892295 http://dx.doi.org/10.1111/1462-2920.13930 Text en © 2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Articles Guccione, Edward J. Kendall, John J. Hitchcock, Andrew Garg, Nitanshu White, Michael A. Mulholland, Francis Poole, Robert K. Kelly, David J. Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability |
title | Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability |
title_full | Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability |
title_fullStr | Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability |
title_full_unstemmed | Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability |
title_short | Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability |
title_sort | transcriptome and proteome dynamics in chemostat culture reveal how campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5656828/ https://www.ncbi.nlm.nih.gov/pubmed/28892295 http://dx.doi.org/10.1111/1462-2920.13930 |
work_keys_str_mv | AT guccioneedwardj transcriptomeandproteomedynamicsinchemostatculturerevealhowcampylobacterjejunimodulatesmetabolismstressresponsesandvirulencefactorsuponchangesinoxygenavailability AT kendalljohnj transcriptomeandproteomedynamicsinchemostatculturerevealhowcampylobacterjejunimodulatesmetabolismstressresponsesandvirulencefactorsuponchangesinoxygenavailability AT hitchcockandrew transcriptomeandproteomedynamicsinchemostatculturerevealhowcampylobacterjejunimodulatesmetabolismstressresponsesandvirulencefactorsuponchangesinoxygenavailability AT gargnitanshu transcriptomeandproteomedynamicsinchemostatculturerevealhowcampylobacterjejunimodulatesmetabolismstressresponsesandvirulencefactorsuponchangesinoxygenavailability AT whitemichaela transcriptomeandproteomedynamicsinchemostatculturerevealhowcampylobacterjejunimodulatesmetabolismstressresponsesandvirulencefactorsuponchangesinoxygenavailability AT mulhollandfrancis transcriptomeandproteomedynamicsinchemostatculturerevealhowcampylobacterjejunimodulatesmetabolismstressresponsesandvirulencefactorsuponchangesinoxygenavailability AT poolerobertk transcriptomeandproteomedynamicsinchemostatculturerevealhowcampylobacterjejunimodulatesmetabolismstressresponsesandvirulencefactorsuponchangesinoxygenavailability AT kellydavidj transcriptomeandproteomedynamicsinchemostatculturerevealhowcampylobacterjejunimodulatesmetabolismstressresponsesandvirulencefactorsuponchangesinoxygenavailability |