Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine

Jin Sun You, Ji Hyun Yong, Gwang Hee Kim, Sungmin Moon, Ki Taek Nam, Ji Hwan Ryu, Mi Young Yoon, Sang Sun Yoon

Research output: Contribution to journalArticle

Abstract

Background: Recent evidence suggests that the commensal microbes act as a barrier against invading pathogens and enteric infections are the consequences of multi-layered interactions among commensals, pathogens, and the host intestinal tissue. However, it remains unclear how perturbations of the gut microbiota compromise host infection resistance, especially through changes at species and metabolite levels. Results: Here, we illustrate how Bacteroides vulgatus, a dominant species of the Bacteroidetes phylum in mouse intestine, suppresses infection by Vibrio cholerae, an important human pathogen. Clindamycin (CL) is an antibiotic that selectively kills anaerobic bacteria, and accordingly Bacteroidetes are completely eradicated from CL-treated mouse intestines. The Bacteroidetes-depleted adult mice developed severe cholera-like symptoms, when infected with V. cholerae. Germ-free mice mono-associated with B. vulgatus became resistant to V. cholerae infection. Levels of V. cholerae growth-inhibitory metabolites including short-chain fatty acids plummeted upon CL treatment, while levels of compounds that enhance V. cholerae proliferation were elevated. Furthermore, the intestinal colonization process of V. cholerae was well-simulated in CL-treated adult mice. Conclusions: Overall, we provide insights into how a symbiotic microbe and a pathogenic intruder interact inside host intestine. We identified B. vulgatus as an indigenous microbial species that can suppress intestinal infection. Our results also demonstrate that commensal-derived metabolites are a critical determinant for host resistance against V. cholerae infection, and that CL pretreatment of adult mice generates a simple yet useful model of cholera infection.

Original languageEnglish
Article number132
JournalMicrobiome
Volume7
Issue number1
DOIs
Publication statusPublished - 2019 Sep 14

Fingerprint

Vibrio cholerae
Intestines
Clindamycin
Bacteroidetes
Vibrio Infections
Infection
Cholera
Bacteroides
Anaerobic Bacteria
Volatile Fatty Acids
Anti-Bacterial Agents
Growth

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Microbiology (medical)

Cite this

You, J. S., Yong, J. H., Kim, G. H., Moon, S., Nam, K. T., Ryu, J. H., ... Yoon, S. S. (2019). Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine. Microbiome, 7(1), [132]. https://doi.org/10.1186/s40168-019-0746-y
You, Jin Sun ; Yong, Ji Hyun ; Kim, Gwang Hee ; Moon, Sungmin ; Nam, Ki Taek ; Ryu, Ji Hwan ; Yoon, Mi Young ; Yoon, Sang Sun. / Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine. In: Microbiome. 2019 ; Vol. 7, No. 1.
@article{320f8aca6e2c4ce9b03ef4b2efc9fb79,
title = "Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine",
abstract = "Background: Recent evidence suggests that the commensal microbes act as a barrier against invading pathogens and enteric infections are the consequences of multi-layered interactions among commensals, pathogens, and the host intestinal tissue. However, it remains unclear how perturbations of the gut microbiota compromise host infection resistance, especially through changes at species and metabolite levels. Results: Here, we illustrate how Bacteroides vulgatus, a dominant species of the Bacteroidetes phylum in mouse intestine, suppresses infection by Vibrio cholerae, an important human pathogen. Clindamycin (CL) is an antibiotic that selectively kills anaerobic bacteria, and accordingly Bacteroidetes are completely eradicated from CL-treated mouse intestines. The Bacteroidetes-depleted adult mice developed severe cholera-like symptoms, when infected with V. cholerae. Germ-free mice mono-associated with B. vulgatus became resistant to V. cholerae infection. Levels of V. cholerae growth-inhibitory metabolites including short-chain fatty acids plummeted upon CL treatment, while levels of compounds that enhance V. cholerae proliferation were elevated. Furthermore, the intestinal colonization process of V. cholerae was well-simulated in CL-treated adult mice. Conclusions: Overall, we provide insights into how a symbiotic microbe and a pathogenic intruder interact inside host intestine. We identified B. vulgatus as an indigenous microbial species that can suppress intestinal infection. Our results also demonstrate that commensal-derived metabolites are a critical determinant for host resistance against V. cholerae infection, and that CL pretreatment of adult mice generates a simple yet useful model of cholera infection.",
author = "You, {Jin Sun} and Yong, {Ji Hyun} and Kim, {Gwang Hee} and Sungmin Moon and Nam, {Ki Taek} and Ryu, {Ji Hwan} and Yoon, {Mi Young} and Yoon, {Sang Sun}",
year = "2019",
month = "9",
day = "14",
doi = "10.1186/s40168-019-0746-y",
language = "English",
volume = "7",
journal = "Microbiome",
issn = "2049-2618",
publisher = "BioMed Central",
number = "1",

}

You, JS, Yong, JH, Kim, GH, Moon, S, Nam, KT, Ryu, JH, Yoon, MY & Yoon, SS 2019, 'Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine', Microbiome, vol. 7, no. 1, 132. https://doi.org/10.1186/s40168-019-0746-y

Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine. / You, Jin Sun; Yong, Ji Hyun; Kim, Gwang Hee; Moon, Sungmin; Nam, Ki Taek; Ryu, Ji Hwan; Yoon, Mi Young; Yoon, Sang Sun.

In: Microbiome, Vol. 7, No. 1, 132, 14.09.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine

AU - You, Jin Sun

AU - Yong, Ji Hyun

AU - Kim, Gwang Hee

AU - Moon, Sungmin

AU - Nam, Ki Taek

AU - Ryu, Ji Hwan

AU - Yoon, Mi Young

AU - Yoon, Sang Sun

PY - 2019/9/14

Y1 - 2019/9/14

N2 - Background: Recent evidence suggests that the commensal microbes act as a barrier against invading pathogens and enteric infections are the consequences of multi-layered interactions among commensals, pathogens, and the host intestinal tissue. However, it remains unclear how perturbations of the gut microbiota compromise host infection resistance, especially through changes at species and metabolite levels. Results: Here, we illustrate how Bacteroides vulgatus, a dominant species of the Bacteroidetes phylum in mouse intestine, suppresses infection by Vibrio cholerae, an important human pathogen. Clindamycin (CL) is an antibiotic that selectively kills anaerobic bacteria, and accordingly Bacteroidetes are completely eradicated from CL-treated mouse intestines. The Bacteroidetes-depleted adult mice developed severe cholera-like symptoms, when infected with V. cholerae. Germ-free mice mono-associated with B. vulgatus became resistant to V. cholerae infection. Levels of V. cholerae growth-inhibitory metabolites including short-chain fatty acids plummeted upon CL treatment, while levels of compounds that enhance V. cholerae proliferation were elevated. Furthermore, the intestinal colonization process of V. cholerae was well-simulated in CL-treated adult mice. Conclusions: Overall, we provide insights into how a symbiotic microbe and a pathogenic intruder interact inside host intestine. We identified B. vulgatus as an indigenous microbial species that can suppress intestinal infection. Our results also demonstrate that commensal-derived metabolites are a critical determinant for host resistance against V. cholerae infection, and that CL pretreatment of adult mice generates a simple yet useful model of cholera infection.

AB - Background: Recent evidence suggests that the commensal microbes act as a barrier against invading pathogens and enteric infections are the consequences of multi-layered interactions among commensals, pathogens, and the host intestinal tissue. However, it remains unclear how perturbations of the gut microbiota compromise host infection resistance, especially through changes at species and metabolite levels. Results: Here, we illustrate how Bacteroides vulgatus, a dominant species of the Bacteroidetes phylum in mouse intestine, suppresses infection by Vibrio cholerae, an important human pathogen. Clindamycin (CL) is an antibiotic that selectively kills anaerobic bacteria, and accordingly Bacteroidetes are completely eradicated from CL-treated mouse intestines. The Bacteroidetes-depleted adult mice developed severe cholera-like symptoms, when infected with V. cholerae. Germ-free mice mono-associated with B. vulgatus became resistant to V. cholerae infection. Levels of V. cholerae growth-inhibitory metabolites including short-chain fatty acids plummeted upon CL treatment, while levels of compounds that enhance V. cholerae proliferation were elevated. Furthermore, the intestinal colonization process of V. cholerae was well-simulated in CL-treated adult mice. Conclusions: Overall, we provide insights into how a symbiotic microbe and a pathogenic intruder interact inside host intestine. We identified B. vulgatus as an indigenous microbial species that can suppress intestinal infection. Our results also demonstrate that commensal-derived metabolites are a critical determinant for host resistance against V. cholerae infection, and that CL pretreatment of adult mice generates a simple yet useful model of cholera infection.

UR - http://www.scopus.com/inward/record.url?scp=85072209450&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85072209450&partnerID=8YFLogxK

U2 - 10.1186/s40168-019-0746-y

DO - 10.1186/s40168-019-0746-y

M3 - Article

C2 - 31521198

AN - SCOPUS:85072209450

VL - 7

JO - Microbiome

JF - Microbiome

SN - 2049-2618

IS - 1

M1 - 132

ER -