Campylobacter jejuni transcriptional and genetic adaptation during human infection

Crofts, Alexander A.; Poly, Frédéric M.; Ewing, Cheryl P.; Kuroiwa, Janelle M.; Rimmer, Joanna E.; Harro, Clayton; Sack, David; Talaat, Kawsar R.; Porter, Chad K.; Gutierrez, Ramiro L.; DeNearing, Barbara; Brubaker, Jessica; Laird, Renée M.; Maue, Alexander C.; Jaep, Kayla; Alcala, Ashley; Tribble, David R.; Riddle, Mark. S.; Ramakrishnan, Amritha; McCoy, Andrea J.; Davies, Bryan W.; Guerry, Patricia; Trent, M. Stephen

doi:10.1038/s41564-018-0133-7

Cited by 85Salmonella and Campylobacter epidemiologyHelicobacter pylori-related gastroenterology studiesBacterial Genetics and Biotechnology

Campylobacter jejuni transcriptional and genetic adaptation during human infection

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Crofts, Alexander A., Poly, Frédéric M., Ewing, Cheryl P., Kuroiwa, Janelle M., Rimmer, Joanna E., Harro, Clayton, Sack, David, Talaat, Kawsar R. +15 more·2018·Nature Microbiology

DOI 10.1038/s41564-018-0133-7PMC PMC5876760

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Abstract

Campylobacter jejuni infections are a leading cause of bacterial food-borne diarrhoeal illness worldwide, and Campylobacter infections in children are associated with stunted growth and therefore long-term deficits into adulthood. Despite this global impact on health and human capital, how zoonotic C. jejuni responds to the human host remains unclear. Unlike other intestinal pathogens, C. jejuni does not harbour pathogen-defining toxins that explicitly contribute to disease in humans. This makes understanding Campylobacter pathogenesis challenging and supports a broad examination of bacterial factors that contribute to C. jejuni infection. Here, we use a controlled human infection model to characterize C. jejuni transcriptional and genetic adaptations in vivo, along with a non-human primate infection model to validate our approach. We found that variation in 11 genes is associated with either acute or persistent human infections and includes products involved in host cell invasion, bile sensing and flagella modification, plus additional potential therapeutic targets. In particular, a functional version of the cell invasion protein A (cipA) gene product is strongly associated with persistently infecting bacteria and we identified its biochemical role in flagella modification. These data characterize the adaptive C. jejuni response to primate infections and suggest therapy design should consider the intrinsic differences between acute and persistently infecting bacteria. In addition, RNA sequencing revealed conserved responses during natural host commensalism and human infections. Thirty-nine genes were differentially regulated in vivo across hosts, lifestyles and C. jejuni strains. This conserved in vivo response highlights important C. jejuni survival mechanisms such as iron acquisition and evasion of the host mucosal immune response. These advances highlight pathogen adaptability across host species and demonstrate the utility of multidisciplinary collaborations in future clinical trials to study pathogens in vivo.

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Campylobacter jejuni encodes genes for heme and iron uptake that are transcribed under iron-limited stress.
“Campylobacter jejuni encodes genes necessary for the uptake of heme and iron that are transcribed under iron-limited stress (Crofts et al., 2018).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Crofts et al., 2018

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Bacterial pathogen adaptation during human infections
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Authors: Crofts, A. A., Poly, F. M., Ewing, C. P., Kuroiwa, J. M., Rimmer, J. E., Harro, C., Sack, D., Talaat, K. R., Porter, C. K., Gutierrez, R. L., DeNearing, B., Brubaker, J., Laird, R. M., Maue, A. C., Jaep, K., Alcala, A., Tribble, D. R., Riddle, M. S., Ramakrishnan, A., McCoy, A. J., Davies, B. W., Guerry, P., & Trent, M. S.
Affiliations: The University of Texas at Austin (US)
Naval Medical Research Command (US)
Johns Hopkins University (US)
Uniformed Services University of the Health Sciences (US)
United States Naval Medical Research Unit SOUTH (PE)
University of Georgia (US)
Corresponding author: Guerry, Patricia
Trent, M. Stephen
ORCID: Crofts, Alexander A.
Poly, Frédéric M.
Ewing, Cheryl P.
Sack, David
Talaat, Kawsar R.
Porter, Chad K.
Laird, Renée M.
Alcala, Ashley
Tribble, David R.
Riddle, Mark. S.
McCoy, Andrea J.
Davies, Bryan W.
Guerry, Patricia
Trent, M. Stephen
Venue: Nature Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2018-03-27
Volume: 3
Issue: 4
Pages: 494-502
ISSN: 2058-5276 (ISSN-L)
DOI: 10.1038/s41564-018-0133-7
PMC: PMC5876760
OpenAlex: W2795318775
Cited by: 85
References: 47
Citations by year: 2026: 6 · 2025: 5 · 2024: 7 · 2023: 10 · 2022: 8 · 2021: 16 · 2020: 17 · 2019: 9 · 2018: 7
FWCI: 11.50
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Microbiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Allergy and Infectious Diseases (R01AI064184, R01AI129940, R01AI076322)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Health Sciences › Medicine › Surgery › Helicobacter pylori-related gastroenterology studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: Campylobacter jejuni, host adaptation, gene expression regulation, persistent infection, acute infection, iron acquisition, controlled human infection model, therapeutic target
MeSH terms: Rifaximin, Animals, Bacterial Proteins, Campylobacter Infections, Chickens, Ciprofloxacin, Flagella, Foodborne Diseases, Humans, Intestines, Membrane Proteins, Genetic Variation, Gene Expression Regulation, Bacterial, Campylobacter jejuni, Azithromycin

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