Cited by 124Vibrio bacteria research studiesEscherichia coli research studiesBacterial Genetics and Biotechnology

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Cholera toxin promotes pathogen acquisition of host-derived nutrients

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Rivera-Chávez, Fabian, Mekalanos, John J.·2019·Nature

DOI 10.1038/s41586-019-1453-3PMC PMC6727848

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Abstract

Vibrio cholerae is the causative agent of cholera, a potentially lethal enteric bacterial infection 1. Cholera toxin (CTX), a protein complex that is secreted by V. cholerae, is required for V. cholerae to cause severe disease. CTX is also thought to promote transmission of the organism, as infected individuals shed many litres of diarrhoeal fluid that typically contains in excess of 10 11 organisms per litre. How the pathogen is able to reach such high concentrations in the intestine during infection remains poorly understood. Here we show that CTX increases pathogen growth and induces a distinct V. cholerae transcriptomic signature that is indicative of an iron-depleted gut niche. During infection, bacterial pathogens need to acquire iron, which is an essential nutrient for growth 2. Most iron in the mammalian host is found in a chelated form within the porphyrin structure of haem, and the ability to use haem as a source of iron is genetically encoded by V. cholerae 3. We show that the genes that enable V. cholerae to obtain iron via haem and vibriobactin confer a growth advantage to the pathogen only when CTX is produced. Furthermore, we found that CTX-induced congestion of capillaries in the terminal ileum correlated with an increased bioavailability of luminal haem. CTX-induced disease in the ileum also led to increased concentrations of long-chain fatty acids and L-lactate metabolites in the lumen, as well as the upregulation of V. cholerae genes that encode enzymes of the tricarboxylic acid (TCA) cycle that contain iron-sulfur clusters. Genetic analysis of V. cholerae suggested that pathogen growth was dependent on the uptake of haem and long-chain fatty acids during infection, but only in a strain capable of producing CTX in vivo. We conclude that CTX-induced disease creates an iron-depleted metabolic niche in the gut, which selectively promotes the growth of V. cholerae through the acquisition of host-derived haem and fatty acids.

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Self-citation

Authors: Rivera-Chávez, F., & Mekalanos, J. J.
Affiliations: Harvard University (US)
Corresponding author: Mekalanos, John J.
ORCID: Rivera-Chávez, Fabian
Mekalanos, John J.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2019-07-31
Volume: 572
Issue: 7768
Pages: 244-248
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-019-1453-3
PMC: PMC6727848
OpenAlex: W2966823177
Cited by: 124
References: 36
Citations by year: 2026: 9 · 2025: 21 · 2024: 16 · 2023: 22 · 2022: 15 · 2021: 24 · 2020: 16 · 2019: 1
FWCI: 9.16
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institutes of Health
National Institute of Allergy and Infectious Diseases (R01AI018045, R37AI018045, T32AI007061)
Topics: Life Sciences › Immunology and Microbiology › Microbiology › Vibrio bacteria research studies
Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: cholera toxin, Vibrio cholerae, long-chain fatty acids, L-lactate, iron-sulfur clusters, TCA cycle, terminal ileum, capillary congestion, bacterial transcriptome, host-pathogen interaction
MeSH terms: Animals, Cholera, Cholera Toxin, Citric Acid Cycle, Fatty Acids, Heme, Rabbits, Vibrio cholerae, Sequence Analysis, RNA, Lactic Acid, Mice, Host-Pathogen Interactions, Transcriptome

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Cholera toxin promotes pathogen acquisition of host-derived nutrients

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