Gut microbiota density influences host physiology and is shaped by host and microbial factors

Eduardo J. Contijoch, Graham J. Britton, Chao Yang, Ilaria Mogno, Zhihua Li, Ruby Ng, Sean R. Llewellyn, Sheela Hira, Crystal Johnson, Keren M. Rabinowitz, Revital Barkan, Iris Dotan, Robert P. Hirten, Shih Chen Fu, Yuying Luo, Nancy Yang, Tramy Luong, Philippe R. Labrias, Sergio Lira, Inga Peter & 54 others Ari Grinspan, Jose C. Clemente, Roman Kosoy, Seunghee Kim-Schulze, Xiaochen Qin, Anabella Castillo, Amanda Hurley, Ashish Atreja, Jason Rogers, Farah Fasihuddin, Merjona Saliaj, Amy Nolan, Pamela Reyes-Mercedes, Carina Rodriguez, Sarah Aly, Kenneth Santa-Cruz, Lauren Peters, Mayte Suárez-Fariñas, Ruiqi Huang, Ke Hao, Jun Zhu, Bin Zhang, Bojan Losic, Haritz Irizar, Won Min Song, Antonio Di Narzo, Wenhui Wang, Benjamin L. Cohen, Christopher DiMaio, David Greenwald, Steven Itzkowitz, Aimee Lucas, James Marion, Elana Maser, Ryan Ungaro, Steven Naymagon, Joshua Novak, Brijen Shah, Thomas A. Ullman, Peter Rubin, James George, Peter Legnani, Shannon E. Telesco, Joshua R. Friedman, Carrie Brodmerkel, Scott Plevy, Judy H. Cho, Jean Frederic Colombel, Eric E. Schadt, Carmen Argmann, Marla Dubinsky, Andrew Kasarskis, Bruce Sands, Jeremiah J. Faith

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

To identify factors that regulate gut microbiota density and the impact of varied microbiota density on health, we assayed this fundamental ecosystem property in fecal samples across mammals, human disease, and therapeutic interventions. Physiologic features of the host (carrying capacity) and the fitness of the gut microbiota shape microbiota density. Therapeutic manipulation of microbiota density in mice altered host metabolic and immune homeostasis. In humans, gut microbiota density was reduced in Crohn's disease, ulcerative colitis, and ileal pouch-anal anastomosis. The gut microbiota in recurrent Clostridium difficile infection had lower density and reduced fitness that were restored by fecal microbiota transplantation. Understanding the interplay between microbiota and disease in terms of microbiota density, host carrying capacity, and microbiota fitness provide new insights into microbiome structure and microbiome targeted therapeutics. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).

Original languageEnglish (US)
JournaleLife
Volume8
DOIs
StatePublished - Jan 22 2019
Externally publishedYes

Fingerprint

Microbiota
Physiology
Clostridium
Mammals
Ecosystems
Conservation of Natural Resources
Health
Clostridium Infections
Colonic Pouches
Peer Review
Clostridium difficile
Gastrointestinal Microbiome
Ulcerative Colitis
Crohn Disease
Ecosystem
Homeostasis
Therapeutics

Keywords

  • fecal microbiota transplantation
  • gut microbiome
  • human
  • human biology
  • infectious disease
  • inflammatory bowel disease
  • medicine
  • microbiology
  • microbiota density
  • mouse

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

Cite this

Contijoch, E. J., Britton, G. J., Yang, C., Mogno, I., Li, Z., Ng, R., ... Faith, J. J. (2019). Gut microbiota density influences host physiology and is shaped by host and microbial factors. eLife, 8. https://doi.org/10.7554/eLife.40553

Gut microbiota density influences host physiology and is shaped by host and microbial factors. / Contijoch, Eduardo J.; Britton, Graham J.; Yang, Chao; Mogno, Ilaria; Li, Zhihua; Ng, Ruby; Llewellyn, Sean R.; Hira, Sheela; Johnson, Crystal; Rabinowitz, Keren M.; Barkan, Revital; Dotan, Iris; Hirten, Robert P.; Fu, Shih Chen; Luo, Yuying; Yang, Nancy; Luong, Tramy; Labrias, Philippe R.; Lira, Sergio; Peter, Inga; Grinspan, Ari; Clemente, Jose C.; Kosoy, Roman; Kim-Schulze, Seunghee; Qin, Xiaochen; Castillo, Anabella; Hurley, Amanda; Atreja, Ashish; Rogers, Jason; Fasihuddin, Farah; Saliaj, Merjona; Nolan, Amy; Reyes-Mercedes, Pamela; Rodriguez, Carina; Aly, Sarah; Santa-Cruz, Kenneth; Peters, Lauren; Suárez-Fariñas, Mayte; Huang, Ruiqi; Hao, Ke; Zhu, Jun; Zhang, Bin; Losic, Bojan; Irizar, Haritz; Song, Won Min; Di Narzo, Antonio; Wang, Wenhui; Cohen, Benjamin L.; DiMaio, Christopher; Greenwald, David; Itzkowitz, Steven; Lucas, Aimee; Marion, James; Maser, Elana; Ungaro, Ryan; Naymagon, Steven; Novak, Joshua; Shah, Brijen; Ullman, Thomas A.; Rubin, Peter; George, James; Legnani, Peter; Telesco, Shannon E.; Friedman, Joshua R.; Brodmerkel, Carrie; Plevy, Scott; Cho, Judy H.; Colombel, Jean Frederic; Schadt, Eric E.; Argmann, Carmen; Dubinsky, Marla; Kasarskis, Andrew; Sands, Bruce; Faith, Jeremiah J.

In: eLife, Vol. 8, 22.01.2019.

Research output: Contribution to journalArticle

Contijoch, EJ, Britton, GJ, Yang, C, Mogno, I, Li, Z, Ng, R, Llewellyn, SR, Hira, S, Johnson, C, Rabinowitz, KM, Barkan, R, Dotan, I, Hirten, RP, Fu, SC, Luo, Y, Yang, N, Luong, T, Labrias, PR, Lira, S, Peter, I, Grinspan, A, Clemente, JC, Kosoy, R, Kim-Schulze, S, Qin, X, Castillo, A, Hurley, A, Atreja, A, Rogers, J, Fasihuddin, F, Saliaj, M, Nolan, A, Reyes-Mercedes, P, Rodriguez, C, Aly, S, Santa-Cruz, K, Peters, L, Suárez-Fariñas, M, Huang, R, Hao, K, Zhu, J, Zhang, B, Losic, B, Irizar, H, Song, WM, Di Narzo, A, Wang, W, Cohen, BL, DiMaio, C, Greenwald, D, Itzkowitz, S, Lucas, A, Marion, J, Maser, E, Ungaro, R, Naymagon, S, Novak, J, Shah, B, Ullman, TA, Rubin, P, George, J, Legnani, P, Telesco, SE, Friedman, JR, Brodmerkel, C, Plevy, S, Cho, JH, Colombel, JF, Schadt, EE, Argmann, C, Dubinsky, M, Kasarskis, A, Sands, B & Faith, JJ 2019, 'Gut microbiota density influences host physiology and is shaped by host and microbial factors', eLife, vol. 8. https://doi.org/10.7554/eLife.40553
Contijoch, Eduardo J. ; Britton, Graham J. ; Yang, Chao ; Mogno, Ilaria ; Li, Zhihua ; Ng, Ruby ; Llewellyn, Sean R. ; Hira, Sheela ; Johnson, Crystal ; Rabinowitz, Keren M. ; Barkan, Revital ; Dotan, Iris ; Hirten, Robert P. ; Fu, Shih Chen ; Luo, Yuying ; Yang, Nancy ; Luong, Tramy ; Labrias, Philippe R. ; Lira, Sergio ; Peter, Inga ; Grinspan, Ari ; Clemente, Jose C. ; Kosoy, Roman ; Kim-Schulze, Seunghee ; Qin, Xiaochen ; Castillo, Anabella ; Hurley, Amanda ; Atreja, Ashish ; Rogers, Jason ; Fasihuddin, Farah ; Saliaj, Merjona ; Nolan, Amy ; Reyes-Mercedes, Pamela ; Rodriguez, Carina ; Aly, Sarah ; Santa-Cruz, Kenneth ; Peters, Lauren ; Suárez-Fariñas, Mayte ; Huang, Ruiqi ; Hao, Ke ; Zhu, Jun ; Zhang, Bin ; Losic, Bojan ; Irizar, Haritz ; Song, Won Min ; Di Narzo, Antonio ; Wang, Wenhui ; Cohen, Benjamin L. ; DiMaio, Christopher ; Greenwald, David ; Itzkowitz, Steven ; Lucas, Aimee ; Marion, James ; Maser, Elana ; Ungaro, Ryan ; Naymagon, Steven ; Novak, Joshua ; Shah, Brijen ; Ullman, Thomas A. ; Rubin, Peter ; George, James ; Legnani, Peter ; Telesco, Shannon E. ; Friedman, Joshua R. ; Brodmerkel, Carrie ; Plevy, Scott ; Cho, Judy H. ; Colombel, Jean Frederic ; Schadt, Eric E. ; Argmann, Carmen ; Dubinsky, Marla ; Kasarskis, Andrew ; Sands, Bruce ; Faith, Jeremiah J. / Gut microbiota density influences host physiology and is shaped by host and microbial factors. In: eLife. 2019 ; Vol. 8.
@article{e92a9691a27b427dbf4ead5f380a8e83,
title = "Gut microbiota density influences host physiology and is shaped by host and microbial factors",
abstract = "To identify factors that regulate gut microbiota density and the impact of varied microbiota density on health, we assayed this fundamental ecosystem property in fecal samples across mammals, human disease, and therapeutic interventions. Physiologic features of the host (carrying capacity) and the fitness of the gut microbiota shape microbiota density. Therapeutic manipulation of microbiota density in mice altered host metabolic and immune homeostasis. In humans, gut microbiota density was reduced in Crohn's disease, ulcerative colitis, and ileal pouch-anal anastomosis. The gut microbiota in recurrent Clostridium difficile infection had lower density and reduced fitness that were restored by fecal microbiota transplantation. Understanding the interplay between microbiota and disease in terms of microbiota density, host carrying capacity, and microbiota fitness provide new insights into microbiome structure and microbiome targeted therapeutics. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).",
keywords = "fecal microbiota transplantation, gut microbiome, human, human biology, infectious disease, inflammatory bowel disease, medicine, microbiology, microbiota density, mouse",
author = "Contijoch, {Eduardo J.} and Britton, {Graham J.} and Chao Yang and Ilaria Mogno and Zhihua Li and Ruby Ng and Llewellyn, {Sean R.} and Sheela Hira and Crystal Johnson and Rabinowitz, {Keren M.} and Revital Barkan and Iris Dotan and Hirten, {Robert P.} and Fu, {Shih Chen} and Yuying Luo and Nancy Yang and Tramy Luong and Labrias, {Philippe R.} and Sergio Lira and Inga Peter and Ari Grinspan and Clemente, {Jose C.} and Roman Kosoy and Seunghee Kim-Schulze and Xiaochen Qin and Anabella Castillo and Amanda Hurley and Ashish Atreja and Jason Rogers and Farah Fasihuddin and Merjona Saliaj and Amy Nolan and Pamela Reyes-Mercedes and Carina Rodriguez and Sarah Aly and Kenneth Santa-Cruz and Lauren Peters and Mayte Su{\'a}rez-Fari{\~n}as and Ruiqi Huang and Ke Hao and Jun Zhu and Bin Zhang and Bojan Losic and Haritz Irizar and Song, {Won Min} and {Di Narzo}, Antonio and Wenhui Wang and Cohen, {Benjamin L.} and Christopher DiMaio and David Greenwald and Steven Itzkowitz and Aimee Lucas and James Marion and Elana Maser and Ryan Ungaro and Steven Naymagon and Joshua Novak and Brijen Shah and Ullman, {Thomas A.} and Peter Rubin and James George and Peter Legnani and Telesco, {Shannon E.} and Friedman, {Joshua R.} and Carrie Brodmerkel and Scott Plevy and Cho, {Judy H.} and Colombel, {Jean Frederic} and Schadt, {Eric E.} and Carmen Argmann and Marla Dubinsky and Andrew Kasarskis and Bruce Sands and Faith, {Jeremiah J.}",
year = "2019",
month = "1",
day = "22",
doi = "10.7554/eLife.40553",
language = "English (US)",
volume = "8",
journal = "eLife",
issn = "2050-084X",
publisher = "eLife Sciences Publications",

}

TY - JOUR

T1 - Gut microbiota density influences host physiology and is shaped by host and microbial factors

AU - Contijoch, Eduardo J.

AU - Britton, Graham J.

AU - Yang, Chao

AU - Mogno, Ilaria

AU - Li, Zhihua

AU - Ng, Ruby

AU - Llewellyn, Sean R.

AU - Hira, Sheela

AU - Johnson, Crystal

AU - Rabinowitz, Keren M.

AU - Barkan, Revital

AU - Dotan, Iris

AU - Hirten, Robert P.

AU - Fu, Shih Chen

AU - Luo, Yuying

AU - Yang, Nancy

AU - Luong, Tramy

AU - Labrias, Philippe R.

AU - Lira, Sergio

AU - Peter, Inga

AU - Grinspan, Ari

AU - Clemente, Jose C.

AU - Kosoy, Roman

AU - Kim-Schulze, Seunghee

AU - Qin, Xiaochen

AU - Castillo, Anabella

AU - Hurley, Amanda

AU - Atreja, Ashish

AU - Rogers, Jason

AU - Fasihuddin, Farah

AU - Saliaj, Merjona

AU - Nolan, Amy

AU - Reyes-Mercedes, Pamela

AU - Rodriguez, Carina

AU - Aly, Sarah

AU - Santa-Cruz, Kenneth

AU - Peters, Lauren

AU - Suárez-Fariñas, Mayte

AU - Huang, Ruiqi

AU - Hao, Ke

AU - Zhu, Jun

AU - Zhang, Bin

AU - Losic, Bojan

AU - Irizar, Haritz

AU - Song, Won Min

AU - Di Narzo, Antonio

AU - Wang, Wenhui

AU - Cohen, Benjamin L.

AU - DiMaio, Christopher

AU - Greenwald, David

AU - Itzkowitz, Steven

AU - Lucas, Aimee

AU - Marion, James

AU - Maser, Elana

AU - Ungaro, Ryan

AU - Naymagon, Steven

AU - Novak, Joshua

AU - Shah, Brijen

AU - Ullman, Thomas A.

AU - Rubin, Peter

AU - George, James

AU - Legnani, Peter

AU - Telesco, Shannon E.

AU - Friedman, Joshua R.

AU - Brodmerkel, Carrie

AU - Plevy, Scott

AU - Cho, Judy H.

AU - Colombel, Jean Frederic

AU - Schadt, Eric E.

AU - Argmann, Carmen

AU - Dubinsky, Marla

AU - Kasarskis, Andrew

AU - Sands, Bruce

AU - Faith, Jeremiah J.

PY - 2019/1/22

Y1 - 2019/1/22

N2 - To identify factors that regulate gut microbiota density and the impact of varied microbiota density on health, we assayed this fundamental ecosystem property in fecal samples across mammals, human disease, and therapeutic interventions. Physiologic features of the host (carrying capacity) and the fitness of the gut microbiota shape microbiota density. Therapeutic manipulation of microbiota density in mice altered host metabolic and immune homeostasis. In humans, gut microbiota density was reduced in Crohn's disease, ulcerative colitis, and ileal pouch-anal anastomosis. The gut microbiota in recurrent Clostridium difficile infection had lower density and reduced fitness that were restored by fecal microbiota transplantation. Understanding the interplay between microbiota and disease in terms of microbiota density, host carrying capacity, and microbiota fitness provide new insights into microbiome structure and microbiome targeted therapeutics. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).

AB - To identify factors that regulate gut microbiota density and the impact of varied microbiota density on health, we assayed this fundamental ecosystem property in fecal samples across mammals, human disease, and therapeutic interventions. Physiologic features of the host (carrying capacity) and the fitness of the gut microbiota shape microbiota density. Therapeutic manipulation of microbiota density in mice altered host metabolic and immune homeostasis. In humans, gut microbiota density was reduced in Crohn's disease, ulcerative colitis, and ileal pouch-anal anastomosis. The gut microbiota in recurrent Clostridium difficile infection had lower density and reduced fitness that were restored by fecal microbiota transplantation. Understanding the interplay between microbiota and disease in terms of microbiota density, host carrying capacity, and microbiota fitness provide new insights into microbiome structure and microbiome targeted therapeutics. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).

KW - fecal microbiota transplantation

KW - gut microbiome

KW - human

KW - human biology

KW - infectious disease

KW - inflammatory bowel disease

KW - medicine

KW - microbiology

KW - microbiota density

KW - mouse

UR - http://www.scopus.com/inward/record.url?scp=85060214409&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85060214409&partnerID=8YFLogxK

U2 - 10.7554/eLife.40553

DO - 10.7554/eLife.40553

M3 - Article

VL - 8

JO - eLife

JF - eLife

SN - 2050-084X

ER -