Infection trains the host for microbiota-enhanced resistance to pathogens

Apollo Stacy; Vinicius Andrade-Oliveira; John A. McCulloch; Benedikt Hild; Ji Hoon Oh; P. Juliana Perez-Chaparro; Choon K. Sim; Ai Ing Lim; Verena M. Link; Michel Enamorado; Giorgio Trinchieri; Julia A. Segre; Barbara Rehermann; Yasmine Belkaid

doi:10.1016/j.cell.2020.12.011

Infection trains the host for microbiota-enhanced resistance to pathogens

Apollo Stacy, Vinicius Andrade-Oliveira, John A. McCulloch, Benedikt Hild, Ji Hoon Oh, P. Juliana Perez-Chaparro, Choon K. Sim, Ai Ing Lim, Verena M. Link, Michel Enamorado, Giorgio Trinchieri, Julia A. Segre, Barbara Rehermann, Yasmine Belkaid

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

104 Scopus citations

Abstract

Previous intestinal infection increases the gut microbiota's resistance to subsequent infection by inhibiting the ability of pathogens to respire.

Original language	English (US)
Pages (from-to)	615-627.e17
Journal	Cell
Volume	184
Issue number	3
DOIs	https://doi.org/10.1016/j.cell.2020.12.011
State	Published - Feb 4 2021
Externally published	Yes

All Science Journal Classification (ASJC) codes

Biochemistry, Genetics and Molecular Biology(all)

Keywords

aerobic respiration
bile acid
bismuth subsalicylate
Citrobacter rodentium
colonization resistance
Enterococcus faecalis
gut microbiome
hydrogen sulfide
Klebsiella pneumoniae
taurine

Access to Document

10.1016/j.cell.2020.12.011

Cite this

@article{7337f5cdaaa540d88f0172441fbf0145,

title = "Infection trains the host for microbiota-enhanced resistance to pathogens",

abstract = "Previous intestinal infection increases the gut microbiota's resistance to subsequent infection by inhibiting the ability of pathogens to respire.",

keywords = "aerobic respiration, bile acid, bismuth subsalicylate, Citrobacter rodentium, colonization resistance, Enterococcus faecalis, gut microbiome, hydrogen sulfide, Klebsiella pneumoniae, taurine",

author = "Apollo Stacy and Vinicius Andrade-Oliveira and McCulloch, {John A.} and Benedikt Hild and Oh, {Ji Hoon} and Perez-Chaparro, {P. Juliana} and Sim, {Choon K.} and Lim, {Ai Ing} and Link, {Verena M.} and Michel Enamorado and Giorgio Trinchieri and Segre, {Julia A.} and Barbara Rehermann and Yasmine Belkaid",

note = "Funding Information: This work was supported by the Intramural Research Programs of NIAID (1ZIAAI001115-11 to Y.B.), NIDDK (1ZIADK054508-22 to B.R.), NCI Center for Cancer Research (1ZIABC011153-11 to G.T.), and NHGRI (1ZIAHG000180-19 to J.A.S.), the NIH Director's Challenge Innovation Award Program (Y.B. and B.R.), the DDIR (Y.B. and B.R.), the NIGMS Postdoctoral Research Associate Training (PRAT) Program (1FI2GM128736-01 to A.S.), the NIH (A.S.), the Pew Latin American Fellows Program (V.A.-O.), the Deutsche Forschungsgemeinschaft (HI 2088/1-1 to B.H.), the Human Frontier Science Program (LT000191/2018 to A.I.L.), and the Cancer Research Institute Irvington Postdoctoral Fellowship Program (M.E.). We thank Xingyao He, Shreni Mistry, and Naisarg Modi (NIAID Microbiome Program); Nicolas Bouladoux, Ejae Lewis, and Dana Trageser-Cesler (NIAID Microbiome Program Gnotobiotic Animal Facility); Kelly Paglia (West Coast Metabolomics Center); Shurjo Sen (NCI Cancer and Inflammation Program); Galina Koroleva (NIH Center for Human Immunology); Kim Webber (Belkaid laboratory), Mirian Krystel De Siqueira (now UCLA), and Austin Hall (now UW-Madison) for technical assistance;Margery Smelkinson (NIAID Biological Imaging Section) for imaging tissue sections; Michael Eckhaus (NIH Division of Veterinary Resources) for scoring liver sections; Krystyna Szymczyk (NIAID Research Technologies Branch) for assisting with E. faecalis identification; Gad Frankel (Imperial College London) for providing C. rodentium ICC169; Andreas B{\"a}umler (UC Davis) for providing pCAL60; the NIAID and NIDDK animal facilities; the NIH HPC Biowulf cluster (https://hpc.nih.gov/); and Les Laboratoires Servier (https://smart.servier.com/). We also thank Ivan Vujkovic-Cvijin and other members of the Belkaid laboratory for providing additional expertise and support. A.S. and Y.B. designed the study and wrote the manuscript; A.S. performed experiments, analyzed 16S and Tn-seq data, and interpreted results; V.A.-O. helped to initiate the study and generated Tn-seq libraries; B.H. J.H.O. and B.R. assisted with wildR mice; J.A.M. and G.T. analyzed shotgun metagenomics and whole-genome-sequencing data; C.K.S. and J.A.S. assisted with the Kpn Tn mutant library; P.J.P.-C. assisted with microbiology experiments; A.I.L. sorted gut epithelial cells; V.M.L analyzed RNA-seq data; and M.E. performed lung infections. NIDDK licensed wildR mice to Taconic Biosciences. Funding Information: This work was supported by the Intramural Research Programs of NIAID ( 1ZIAAI001115-11 to Y.B.), NIDDK ( 1ZIADK054508-22 to B.R.), NCI Center for Cancer Research ( 1ZIABC011153-11 to G.T.), and NHGRI ( 1ZIAHG000180-19 to J.A.S.), the NIH Director{\textquoteright}s Challenge Innovation Award Program (Y.B. and B.R.), the DDIR (Y.B. and B.R.), the NIGMS Postdoctoral Research Associate Training (PRAT) Program ( 1FI2GM128736-01 to A.S.), the NIH (A.S.), the Pew Latin American Fellows Program (V.A.-O.), the Deutsche Forschungsgemeinschaft ( HI 2088/1-1 to B.H.), the Human Frontier Science Program ( LT000191/2018 to A.I.L.), and the Cancer Research Institute Irvington Postdoctoral Fellowship Program (M.E.). We thank Xingyao He, Shreni Mistry, and Naisarg Modi (NIAID Microbiome Program); Nicolas Bouladoux, Ejae Lewis, and Dana Trageser-Cesler (NIAID Microbiome Program Gnotobiotic Animal Facility); Kelly Paglia (West Coast Metabolomics Center); Shurjo Sen (NCI Cancer and Inflammation Program); Galina Koroleva (NIH Center for Human Immunology); Kim Webber (Belkaid laboratory), Mirian Krystel De Siqueira (now UCLA), and Austin Hall (now UW-Madison) for technical assistance;Margery Smelkinson (NIAID Biological Imaging Section) for imaging tissue sections; Michael Eckhaus (NIH Division of Veterinary Resources) for scoring liver sections; Krystyna Szymczyk (NIAID Research Technologies Branch) for assisting with E. faecalis identification; Gad Frankel (Imperial College London) for providing C. rodentium ICC169; Andreas B{\"a}umler (UC Davis) for providing pCAL60; the NIAID and NIDDK animal facilities; the NIH HPC Biowulf cluster ( https://hpc.nih.gov/ ); and Les Laboratoires Servier ( https://smart.servier.com/ ). We also thank Ivan Vujkovic-Cvijin and other members of the Belkaid laboratory for providing additional expertise and support. Publisher Copyright: {\textcopyright} 2020",

year = "2021",

month = feb,

day = "4",

doi = "10.1016/j.cell.2020.12.011",

language = "English (US)",

volume = "184",

pages = "615--627.e17",

journal = "Cell",

issn = "0092-8674",

publisher = "Cell Press",

number = "3",

}

TY - JOUR

T1 - Infection trains the host for microbiota-enhanced resistance to pathogens

AU - Stacy, Apollo

AU - Andrade-Oliveira, Vinicius

AU - McCulloch, John A.

AU - Hild, Benedikt

AU - Oh, Ji Hoon

AU - Perez-Chaparro, P. Juliana

AU - Sim, Choon K.

AU - Lim, Ai Ing

AU - Link, Verena M.

AU - Enamorado, Michel

AU - Trinchieri, Giorgio

AU - Segre, Julia A.

AU - Rehermann, Barbara

AU - Belkaid, Yasmine

N1 - Funding Information: This work was supported by the Intramural Research Programs of NIAID (1ZIAAI001115-11 to Y.B.), NIDDK (1ZIADK054508-22 to B.R.), NCI Center for Cancer Research (1ZIABC011153-11 to G.T.), and NHGRI (1ZIAHG000180-19 to J.A.S.), the NIH Director's Challenge Innovation Award Program (Y.B. and B.R.), the DDIR (Y.B. and B.R.), the NIGMS Postdoctoral Research Associate Training (PRAT) Program (1FI2GM128736-01 to A.S.), the NIH (A.S.), the Pew Latin American Fellows Program (V.A.-O.), the Deutsche Forschungsgemeinschaft (HI 2088/1-1 to B.H.), the Human Frontier Science Program (LT000191/2018 to A.I.L.), and the Cancer Research Institute Irvington Postdoctoral Fellowship Program (M.E.). We thank Xingyao He, Shreni Mistry, and Naisarg Modi (NIAID Microbiome Program); Nicolas Bouladoux, Ejae Lewis, and Dana Trageser-Cesler (NIAID Microbiome Program Gnotobiotic Animal Facility); Kelly Paglia (West Coast Metabolomics Center); Shurjo Sen (NCI Cancer and Inflammation Program); Galina Koroleva (NIH Center for Human Immunology); Kim Webber (Belkaid laboratory), Mirian Krystel De Siqueira (now UCLA), and Austin Hall (now UW-Madison) for technical assistance;Margery Smelkinson (NIAID Biological Imaging Section) for imaging tissue sections; Michael Eckhaus (NIH Division of Veterinary Resources) for scoring liver sections; Krystyna Szymczyk (NIAID Research Technologies Branch) for assisting with E. faecalis identification; Gad Frankel (Imperial College London) for providing C. rodentium ICC169; Andreas Bäumler (UC Davis) for providing pCAL60; the NIAID and NIDDK animal facilities; the NIH HPC Biowulf cluster (https://hpc.nih.gov/); and Les Laboratoires Servier (https://smart.servier.com/). We also thank Ivan Vujkovic-Cvijin and other members of the Belkaid laboratory for providing additional expertise and support. A.S. and Y.B. designed the study and wrote the manuscript; A.S. performed experiments, analyzed 16S and Tn-seq data, and interpreted results; V.A.-O. helped to initiate the study and generated Tn-seq libraries; B.H. J.H.O. and B.R. assisted with wildR mice; J.A.M. and G.T. analyzed shotgun metagenomics and whole-genome-sequencing data; C.K.S. and J.A.S. assisted with the Kpn Tn mutant library; P.J.P.-C. assisted with microbiology experiments; A.I.L. sorted gut epithelial cells; V.M.L analyzed RNA-seq data; and M.E. performed lung infections. NIDDK licensed wildR mice to Taconic Biosciences. Funding Information: This work was supported by the Intramural Research Programs of NIAID ( 1ZIAAI001115-11 to Y.B.), NIDDK ( 1ZIADK054508-22 to B.R.), NCI Center for Cancer Research ( 1ZIABC011153-11 to G.T.), and NHGRI ( 1ZIAHG000180-19 to J.A.S.), the NIH Director’s Challenge Innovation Award Program (Y.B. and B.R.), the DDIR (Y.B. and B.R.), the NIGMS Postdoctoral Research Associate Training (PRAT) Program ( 1FI2GM128736-01 to A.S.), the NIH (A.S.), the Pew Latin American Fellows Program (V.A.-O.), the Deutsche Forschungsgemeinschaft ( HI 2088/1-1 to B.H.), the Human Frontier Science Program ( LT000191/2018 to A.I.L.), and the Cancer Research Institute Irvington Postdoctoral Fellowship Program (M.E.). We thank Xingyao He, Shreni Mistry, and Naisarg Modi (NIAID Microbiome Program); Nicolas Bouladoux, Ejae Lewis, and Dana Trageser-Cesler (NIAID Microbiome Program Gnotobiotic Animal Facility); Kelly Paglia (West Coast Metabolomics Center); Shurjo Sen (NCI Cancer and Inflammation Program); Galina Koroleva (NIH Center for Human Immunology); Kim Webber (Belkaid laboratory), Mirian Krystel De Siqueira (now UCLA), and Austin Hall (now UW-Madison) for technical assistance;Margery Smelkinson (NIAID Biological Imaging Section) for imaging tissue sections; Michael Eckhaus (NIH Division of Veterinary Resources) for scoring liver sections; Krystyna Szymczyk (NIAID Research Technologies Branch) for assisting with E. faecalis identification; Gad Frankel (Imperial College London) for providing C. rodentium ICC169; Andreas Bäumler (UC Davis) for providing pCAL60; the NIAID and NIDDK animal facilities; the NIH HPC Biowulf cluster ( https://hpc.nih.gov/ ); and Les Laboratoires Servier ( https://smart.servier.com/ ). We also thank Ivan Vujkovic-Cvijin and other members of the Belkaid laboratory for providing additional expertise and support. Publisher Copyright: © 2020

PY - 2021/2/4

Y1 - 2021/2/4

N2 - Previous intestinal infection increases the gut microbiota's resistance to subsequent infection by inhibiting the ability of pathogens to respire.

AB - Previous intestinal infection increases the gut microbiota's resistance to subsequent infection by inhibiting the ability of pathogens to respire.

KW - aerobic respiration

KW - bile acid

KW - bismuth subsalicylate

KW - Citrobacter rodentium

KW - colonization resistance

KW - Enterococcus faecalis

KW - gut microbiome

KW - hydrogen sulfide

KW - Klebsiella pneumoniae

KW - taurine

UR - http://www.scopus.com/inward/record.url?scp=85099559534&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85099559534&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2020.12.011

DO - 10.1016/j.cell.2020.12.011

M3 - Article

C2 - 33453153

AN - SCOPUS:85099559534

SN - 0092-8674

VL - 184

SP - 615-627.e17

JO - Cell

JF - Cell

IS - 3

ER -

Infection trains the host for microbiota-enhanced resistance to pathogens

Abstract

All Science Journal Classification (ASJC) codes

Keywords

Access to Document

Other files and links

Fingerprint

Cite this