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Avian Intestinal Mucus Modulates Campylobacter jejuni Gene Expression in a Host-Specific Manner

Campylobacter jejuni is a leading cause of bacterial foodborne illness in humans worldwide. However, C. jejuni naturally colonizes poultry without causing pathology where it resides deep within mucus of the cecal crypts. Mucus may modulate the pathogenicity of C. jejuni in a species-specific manner,...

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Autores principales: Looft, Torey, Cai, Guohong, Choudhury, Biswa, Lai, Lisa X., Lippolis, John D., Reinhardt, Timothy A., Sylte, Matthew J., Casey, Thomas A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6338021/
https://www.ncbi.nlm.nih.gov/pubmed/30687245
http://dx.doi.org/10.3389/fmicb.2018.03215
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author Looft, Torey
Cai, Guohong
Choudhury, Biswa
Lai, Lisa X.
Lippolis, John D.
Reinhardt, Timothy A.
Sylte, Matthew J.
Casey, Thomas A.
author_facet Looft, Torey
Cai, Guohong
Choudhury, Biswa
Lai, Lisa X.
Lippolis, John D.
Reinhardt, Timothy A.
Sylte, Matthew J.
Casey, Thomas A.
author_sort Looft, Torey
collection PubMed
description Campylobacter jejuni is a leading cause of bacterial foodborne illness in humans worldwide. However, C. jejuni naturally colonizes poultry without causing pathology where it resides deep within mucus of the cecal crypts. Mucus may modulate the pathogenicity of C. jejuni in a species-specific manner, where it is pathogenic in humans and asymptomatic in poultry. Little is known about how intestinal mucus from different host species affects C. jejuni gene expression. In this study we characterized the growth and transcriptome of C. jejuni NCTC11168 cultured in defined media supplemented with or without mucus isolated from avian (chicken or turkey) or mammalian (cow, pig, or sheep) sources. C. jejuni showed substantially improved growth over defined media, with mucus from all species, showing that intestinal mucus was an energy source for C. jejuni. Seventy-three genes were differentially expressed when C. jejuni was cultured in avian vs. mammalian mucus. Genes associated with iron acquisition and resistance to oxidative stress were significantly increased in avian mucus. Many of the differentially expressed genes were flanked by differentially expressed antisense RNA asRNA, suggesting a role in gene regulation. This study highlights the interactions between C. jejuni and host mucus and the impact on gene expression, growth and invasion of host cells, suggesting important responses to environmental cues that facilitate intestinal colonization. IMPORTANCE  Campylobacter jejuni infection of humans is an important health problem world-wide and is the leading bacterial cause of foodborne illnesses in U.S. The main route for exposure for humans is consumption of poultry meat contaminated during processing. C. jejuni is frequently found in poultry, residing within the mucus of the intestinal tract without causing disease. It is not clear why C. jejuni causes disease in some animals and humans, while leaving birds without symptoms. To understand its activity in birds, we characterized C. jejuni responses to poultry mucus to identify genes turned on in the intestinal tract of birds. We identified genes important for colonization and persistence within the poultry gut, turned on when C. jejuni was exposed to poultry mucus. Our findings are an important step in understanding how C. jejuni responds and interacts in the poultry gut, and may identify ways to reduce C. jejuni in birds.
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spelling pubmed-63380212019-01-25 Avian Intestinal Mucus Modulates Campylobacter jejuni Gene Expression in a Host-Specific Manner Looft, Torey Cai, Guohong Choudhury, Biswa Lai, Lisa X. Lippolis, John D. Reinhardt, Timothy A. Sylte, Matthew J. Casey, Thomas A. Front Microbiol Microbiology Campylobacter jejuni is a leading cause of bacterial foodborne illness in humans worldwide. However, C. jejuni naturally colonizes poultry without causing pathology where it resides deep within mucus of the cecal crypts. Mucus may modulate the pathogenicity of C. jejuni in a species-specific manner, where it is pathogenic in humans and asymptomatic in poultry. Little is known about how intestinal mucus from different host species affects C. jejuni gene expression. In this study we characterized the growth and transcriptome of C. jejuni NCTC11168 cultured in defined media supplemented with or without mucus isolated from avian (chicken or turkey) or mammalian (cow, pig, or sheep) sources. C. jejuni showed substantially improved growth over defined media, with mucus from all species, showing that intestinal mucus was an energy source for C. jejuni. Seventy-three genes were differentially expressed when C. jejuni was cultured in avian vs. mammalian mucus. Genes associated with iron acquisition and resistance to oxidative stress were significantly increased in avian mucus. Many of the differentially expressed genes were flanked by differentially expressed antisense RNA asRNA, suggesting a role in gene regulation. This study highlights the interactions between C. jejuni and host mucus and the impact on gene expression, growth and invasion of host cells, suggesting important responses to environmental cues that facilitate intestinal colonization. IMPORTANCE  Campylobacter jejuni infection of humans is an important health problem world-wide and is the leading bacterial cause of foodborne illnesses in U.S. The main route for exposure for humans is consumption of poultry meat contaminated during processing. C. jejuni is frequently found in poultry, residing within the mucus of the intestinal tract without causing disease. It is not clear why C. jejuni causes disease in some animals and humans, while leaving birds without symptoms. To understand its activity in birds, we characterized C. jejuni responses to poultry mucus to identify genes turned on in the intestinal tract of birds. We identified genes important for colonization and persistence within the poultry gut, turned on when C. jejuni was exposed to poultry mucus. Our findings are an important step in understanding how C. jejuni responds and interacts in the poultry gut, and may identify ways to reduce C. jejuni in birds. Frontiers Media S.A. 2019-01-07 /pmc/articles/PMC6338021/ /pubmed/30687245 http://dx.doi.org/10.3389/fmicb.2018.03215 Text en Copyright © 2019 Looft, Cai, Choudhury, Lai, Lippolis, Reinhardt, Sylte and Casey. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Looft, Torey
Cai, Guohong
Choudhury, Biswa
Lai, Lisa X.
Lippolis, John D.
Reinhardt, Timothy A.
Sylte, Matthew J.
Casey, Thomas A.
Avian Intestinal Mucus Modulates Campylobacter jejuni Gene Expression in a Host-Specific Manner
title Avian Intestinal Mucus Modulates Campylobacter jejuni Gene Expression in a Host-Specific Manner
title_full Avian Intestinal Mucus Modulates Campylobacter jejuni Gene Expression in a Host-Specific Manner
title_fullStr Avian Intestinal Mucus Modulates Campylobacter jejuni Gene Expression in a Host-Specific Manner
title_full_unstemmed Avian Intestinal Mucus Modulates Campylobacter jejuni Gene Expression in a Host-Specific Manner
title_short Avian Intestinal Mucus Modulates Campylobacter jejuni Gene Expression in a Host-Specific Manner
title_sort avian intestinal mucus modulates campylobacter jejuni gene expression in a host-specific manner
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6338021/
https://www.ncbi.nlm.nih.gov/pubmed/30687245
http://dx.doi.org/10.3389/fmicb.2018.03215
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