Pathogenic E. coli Extracts Nutrients from Infected Host Cells Utilizing Injectisome Components

Ritesh Ranjan Pal; Amit K. Baidya; Gideon Mamou; Saurabh Bhattacharya; Yaakov Socol; Simi Kobi; Naama Katsowich; Sigal Ben-Yehuda; Ilan Rosenshine

doi:10.1016/j.cell.2019.02.022

Pathogenic E. coli Extracts Nutrients from Infected Host Cells Utilizing Injectisome Components

Ritesh Ranjan Pal, Amit K. Baidya, Gideon Mamou, Saurabh Bhattacharya, Yaakov Socol, Simi Kobi, Naama Katsowich, Sigal Ben-Yehuda^*, Ilan Rosenshine

^*Corresponding author for this work

Department of Microbiology and Molecular Genetics

Research output: Contribution to journal › Article › peer-review

45 Scopus citations

Abstract

Microbiota and intestinal epithelium restrict pathogen growth by rapid nutrient consumption. We investigated how pathogens circumvent this obstacle to colonize the host. Utilizing enteropathogenic E. coli (EPEC), we show that host-attached bacteria obtain nutrients from infected host cell in a process we termed host nutrient extraction (HNE). We identified an inner-membrane protein complex, henceforth termed CORE, as necessary and sufficient for HNE. The CORE is a key component of the EPEC injectisome, however, here we show that it supports the formation of an alternative structure, composed of membranous nanotubes, protruding from the EPEC surface to directly contact the host. The injectisome and flagellum are evolutionarily related, both containing conserved COREs. Remarkably, CORE complexes of diverse ancestries, including distant flagellar COREs, could rescue HNE capacity of EPEC lacking its native CORE. Our results support the notion that HNE is a widespread virulence strategy, enabling pathogens to thrive in competitive niches.

Original language	American English
Pages (from-to)	683-696.e18
Journal	Cell
Volume	177
Issue number	3
DOIs	https://doi.org/10.1016/j.cell.2019.02.022
State	Published - 18 Apr 2019

Bibliographical note

Funding Information:
We thank E. Blayvas and A. Ben-Hur (Hebrew University, IL) for help with XHR-SEM analyses. We are grateful to S. Wagner (Tubingen University, Germany) for providing a file used to generate Figure 4 A and A. Rouvinski (Hebrew University, IL) for valuable insights. We are indebted to members of the Ben-Yehuda and Rosenshine laboratories for valuable discussions and comments. This work was supported by the European Research Council (ERC) ( 339984 to S.B.-Y.), European Union; a grant from the Israel Science Foundation ( 617/15 to I.R.), Israel; and ERC Synergy ( 810186 to S.B.-Y. and I.R.), European Union.

Publisher Copyright:
© 2019 Elsevier Inc.

Keywords

EPEC
T3SS
enteropathogenic E. coli
export apparatus
flagella
host nutrient extraction
host-pathogen interaction
injectisome
nanotubes
type III secretion system

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10.1016/j.cell.2019.02.022

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title = "Pathogenic E. coli Extracts Nutrients from Infected Host Cells Utilizing Injectisome Components",

abstract = "Microbiota and intestinal epithelium restrict pathogen growth by rapid nutrient consumption. We investigated how pathogens circumvent this obstacle to colonize the host. Utilizing enteropathogenic E. coli (EPEC), we show that host-attached bacteria obtain nutrients from infected host cell in a process we termed host nutrient extraction (HNE). We identified an inner-membrane protein complex, henceforth termed CORE, as necessary and sufficient for HNE. The CORE is a key component of the EPEC injectisome, however, here we show that it supports the formation of an alternative structure, composed of membranous nanotubes, protruding from the EPEC surface to directly contact the host. The injectisome and flagellum are evolutionarily related, both containing conserved COREs. Remarkably, CORE complexes of diverse ancestries, including distant flagellar COREs, could rescue HNE capacity of EPEC lacking its native CORE. Our results support the notion that HNE is a widespread virulence strategy, enabling pathogens to thrive in competitive niches.",

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author = "Pal, {Ritesh Ranjan} and Baidya, {Amit K.} and Gideon Mamou and Saurabh Bhattacharya and Yaakov Socol and Simi Kobi and Naama Katsowich and Sigal Ben-Yehuda and Ilan Rosenshine",

note = "Funding Information: We thank E. Blayvas and A. Ben-Hur (Hebrew University, IL) for help with XHR-SEM analyses. We are grateful to S. Wagner (Tubingen University, Germany) for providing a file used to generate Figure 4 A and A. Rouvinski (Hebrew University, IL) for valuable insights. We are indebted to members of the Ben-Yehuda and Rosenshine laboratories for valuable discussions and comments. This work was supported by the European Research Council (ERC) ( 339984 to S.B.-Y.), European Union; a grant from the Israel Science Foundation ( 617/15 to I.R.), Israel; and ERC Synergy ( 810186 to S.B.-Y. and I.R.), European Union. Publisher Copyright: {\textcopyright} 2019 Elsevier Inc.",

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AU - Bhattacharya, Saurabh

AU - Socol, Yaakov

AU - Kobi, Simi

AU - Katsowich, Naama

AU - Ben-Yehuda, Sigal

AU - Rosenshine, Ilan

N1 - Funding Information: We thank E. Blayvas and A. Ben-Hur (Hebrew University, IL) for help with XHR-SEM analyses. We are grateful to S. Wagner (Tubingen University, Germany) for providing a file used to generate Figure 4 A and A. Rouvinski (Hebrew University, IL) for valuable insights. We are indebted to members of the Ben-Yehuda and Rosenshine laboratories for valuable discussions and comments. This work was supported by the European Research Council (ERC) ( 339984 to S.B.-Y.), European Union; a grant from the Israel Science Foundation ( 617/15 to I.R.), Israel; and ERC Synergy ( 810186 to S.B.-Y. and I.R.), European Union. Publisher Copyright: © 2019 Elsevier Inc.

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N2 - Microbiota and intestinal epithelium restrict pathogen growth by rapid nutrient consumption. We investigated how pathogens circumvent this obstacle to colonize the host. Utilizing enteropathogenic E. coli (EPEC), we show that host-attached bacteria obtain nutrients from infected host cell in a process we termed host nutrient extraction (HNE). We identified an inner-membrane protein complex, henceforth termed CORE, as necessary and sufficient for HNE. The CORE is a key component of the EPEC injectisome, however, here we show that it supports the formation of an alternative structure, composed of membranous nanotubes, protruding from the EPEC surface to directly contact the host. The injectisome and flagellum are evolutionarily related, both containing conserved COREs. Remarkably, CORE complexes of diverse ancestries, including distant flagellar COREs, could rescue HNE capacity of EPEC lacking its native CORE. Our results support the notion that HNE is a widespread virulence strategy, enabling pathogens to thrive in competitive niches.

AB - Microbiota and intestinal epithelium restrict pathogen growth by rapid nutrient consumption. We investigated how pathogens circumvent this obstacle to colonize the host. Utilizing enteropathogenic E. coli (EPEC), we show that host-attached bacteria obtain nutrients from infected host cell in a process we termed host nutrient extraction (HNE). We identified an inner-membrane protein complex, henceforth termed CORE, as necessary and sufficient for HNE. The CORE is a key component of the EPEC injectisome, however, here we show that it supports the formation of an alternative structure, composed of membranous nanotubes, protruding from the EPEC surface to directly contact the host. The injectisome and flagellum are evolutionarily related, both containing conserved COREs. Remarkably, CORE complexes of diverse ancestries, including distant flagellar COREs, could rescue HNE capacity of EPEC lacking its native CORE. Our results support the notion that HNE is a widespread virulence strategy, enabling pathogens to thrive in competitive niches.

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KW - T3SS

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KW - export apparatus

KW - flagella

KW - host nutrient extraction

KW - host-pathogen interaction

KW - injectisome

KW - nanotubes

KW - type III secretion system

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DO - 10.1016/j.cell.2019.02.022

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SN - 0092-8674

VL - 177

SP - 683-696.e18

JO - Cell

JF - Cell

IS - 3

ER -

Pathogenic E. coli Extracts Nutrients from Infected Host Cells Utilizing Injectisome Components

Abstract

Bibliographical note

Keywords

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