Microbial Respiration and Formate Oxidation as Metabolic Signatures of Inflammation-Associated Dysbiosis

Elizabeth R. Hughes, Maria G. Winter, Breck A. Duerkop, Luisella Spiga, Tatiane Furtado de Carvalho, Wenhan Zhu, Caroline C. Gillis, Lisa Büttner, Madeline P. Smoot, Cassie L. Behrendt, Sara Cherry, Renato L. Santos, Lora V. Hooper, Sebastian E. Winter

Research output: Contribution to journalArticle

50 Citations (Scopus)

Abstract

Intestinal inflammation is frequently associated with an alteration of the gut microbiota, termed dysbiosis, which is characterized by a reduced abundance of obligate anaerobic bacteria and an expansion of facultative Proteobacteria such as commensal E. coli. The mechanisms enabling the outgrowth of Proteobacteria during inflammation are incompletely understood. Metagenomic sequencing revealed bacterial formate oxidation and aerobic respiration to be overrepresented metabolic pathways in a chemically induced murine model of colitis. Dysbiosis was accompanied by increased formate levels in the gut lumen. Formate was of microbial origin since no formate was detected in germ-free mice. Complementary studies using commensal E. coli strains as model organisms indicated that formate dehydrogenase and terminal oxidase genes provided a fitness advantage in murine models of colitis. In vivo, formate served as electron donor in conjunction with oxygen as the terminal electron acceptor. This work identifies bacterial formate oxidation and oxygen respiration as metabolic signatures for inflammation-associated dysbiosis.

Original languageEnglish (US)
Pages (from-to)208-219
Number of pages12
JournalCell Host and Microbe
Volume21
Issue number2
DOIs
StatePublished - Feb 8 2017

Fingerprint

formic acid
Dysbiosis
Respiration
Inflammation
Proteobacteria
Colitis
Formate Dehydrogenases
Electrons
Oxygen
Escherichia coli
Metagenomics
Anaerobic Bacteria
Metabolic Networks and Pathways
Oxidoreductases

Keywords

  • bacterial respiration
  • dysbiosis
  • formate metabolism
  • gut microbiota
  • intestinal inflammation
  • metagenomics

ASJC Scopus subject areas

  • Molecular Biology
  • Immunology and Microbiology(all)
  • Cancer Research

Cite this

Microbial Respiration and Formate Oxidation as Metabolic Signatures of Inflammation-Associated Dysbiosis. / Hughes, Elizabeth R.; Winter, Maria G.; Duerkop, Breck A.; Spiga, Luisella; Furtado de Carvalho, Tatiane; Zhu, Wenhan; Gillis, Caroline C.; Büttner, Lisa; Smoot, Madeline P.; Behrendt, Cassie L.; Cherry, Sara; Santos, Renato L.; Hooper, Lora V.; Winter, Sebastian E.

In: Cell Host and Microbe, Vol. 21, No. 2, 08.02.2017, p. 208-219.

Research output: Contribution to journalArticle

Hughes, ER, Winter, MG, Duerkop, BA, Spiga, L, Furtado de Carvalho, T, Zhu, W, Gillis, CC, Büttner, L, Smoot, MP, Behrendt, CL, Cherry, S, Santos, RL, Hooper, LV & Winter, SE 2017, 'Microbial Respiration and Formate Oxidation as Metabolic Signatures of Inflammation-Associated Dysbiosis', Cell Host and Microbe, vol. 21, no. 2, pp. 208-219. https://doi.org/10.1016/j.chom.2017.01.005
Hughes, Elizabeth R. ; Winter, Maria G. ; Duerkop, Breck A. ; Spiga, Luisella ; Furtado de Carvalho, Tatiane ; Zhu, Wenhan ; Gillis, Caroline C. ; Büttner, Lisa ; Smoot, Madeline P. ; Behrendt, Cassie L. ; Cherry, Sara ; Santos, Renato L. ; Hooper, Lora V. ; Winter, Sebastian E. / Microbial Respiration and Formate Oxidation as Metabolic Signatures of Inflammation-Associated Dysbiosis. In: Cell Host and Microbe. 2017 ; Vol. 21, No. 2. pp. 208-219.
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