Strain-level fitness in the gut microbiome is an emergent property of glycans and a single metabolite.

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Tytuł:: Strain-level fitness in the gut microbiome is an emergent property of glycans and a single metabolite.
Autorzy:: Park SY; Division of Infectious Diseases and Division of Gastroenterology, Department of Pediatrics, Boston Children's Hospital, Boston, MA, USA.
Rao C; Division of Infectious Diseases and Division of Gastroenterology, Department of Pediatrics, Boston Children's Hospital, Boston, MA, USA.
Coyte KZ; Division of Infectious Diseases and Division of Gastroenterology, Department of Pediatrics, Boston Children's Hospital, Boston, MA, USA.
Kuziel GA; Division of Infectious Diseases and Division of Gastroenterology, Department of Pediatrics, Boston Children's Hospital, Boston, MA, USA.
Zhang Y; Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA; Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Huang W; Whitehead Institute for Biomedical Research, Cambridge, MA, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
Franzosa EA; Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Weng JK; Whitehead Institute for Biomedical Research, Cambridge, MA, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
Huttenhower C; Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA; Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Rakoff-Nahoum S; Division of Infectious Diseases and Division of Gastroenterology, Department of Pediatrics, Boston Children's Hospital, Boston, MA, USA; Department of Microbiology, Harvard Medical School, Boston, MA, USA; Broad Institute of MIT and Harvard, Cambridge, MA, USA. Electronic address: .
Źródło:: Cell [Cell] 2022 Feb 03; Vol. 185 (3), pp. 513-529.e21.
Typ publikacji:: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Publication: Cambridge, Ma : Cell Press
Original Publication: Cambridge, MIT Press.
MeSH Terms:: Gastrointestinal Microbiome*/drug effects
Gastrointestinal Microbiome*/genetics
Metabolome*/drug effects
Metabolome*/genetics
Polysaccharides/*metabolism
Acyl Coenzyme A/metabolism ; Amino Acid Sequence ; Amino Acids, Branched-Chain/metabolism ; Bacteroidetes/drug effects ; Bacteroidetes/genetics ; Bacteroidetes/growth & development ; Butyrates/chemistry ; Butyrates/pharmacology ; Coenzyme A-Transferases/chemistry ; Coenzyme A-Transferases/metabolism ; Genetic Variation/drug effects ; Hydrogen-Ion Concentration ; Polymorphism, Single Nucleotide/genetics ; Promoter Regions, Genetic/genetics ; Species Specificity ; Stress, Physiological/drug effects ; Stress, Physiological/genetics ; Transcription, Genetic/drug effects
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Grant Information:: P30 DK034854 United States DK NIDDK NIH HHS; DP2 GM136652 United States GM NIGMS NIH HHS; R24 DK110499 United States DK NIDDK NIH HHS; K08 AI130392 United States AI NIAID NIH HHS; United Kingdom WT_ Wellcome Trust
Contributed Indexing:: Keywords: Acyl-CoA metabolism; Bacteroides; butyrate; core genome; diet; emergent properties; fitness; glycans; gut microbiome; sugars
Substance Nomenclature:: 0 (Acyl Coenzyme A)
0 (Amino Acids, Branched-Chain)
0 (Butyrates)
0 (Polysaccharides)
EC 2.8.3.- (Coenzyme A-Transferases)
EC 2.8.3.- (acyl-CoA transferase)
Entry Date(s):: Date Created: 20220205 Date Completed: 20220224 Latest Revision: 20230204
Update Code:: 20240104
PubMed Central ID:: PMC8896310
DOI:: 10.1016/j.cell.2022.01.002
PMID:: 35120663
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The human gut microbiota resides within a diverse chemical environment challenging our ability to understand the forces shaping this ecosystem. Here, we reveal that fitness of the Bacteroidales, the dominant order of bacteria in the human gut, is an emergent property of glycans and one specific metabolite, butyrate. Distinct sugars serve as strain-variable fitness switches activating context-dependent inhibitory functions of butyrate. Differential fitness effects of butyrate within the Bacteroides are mediated by species-level variation in Acyl-CoA thioesterase activity and nucleotide polymorphisms regulating an Acyl-CoA transferase. Using in vivo multi-omic profiles, we demonstrate Bacteroides fitness in the human gut is associated together, but not independently, with Acyl-CoA transferase expression and butyrate. Our data reveal that each strain of the Bacteroides exists within a unique fitness landscape based on the interaction of chemical components unpredictable by the effect of each part alone mediated by flexibility in the core genome.
Competing Interests: Declaration of interests J.K.W. is a member of the SAB and a shareholder of DoubleRainbow Biosciences, Galixir, and Inari Agriculture. The other authors declare no competing interests.
(Copyright © 2022 Elsevier Inc. All rights reserved.)

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