Genetic manipulation of gut microbes enables single-gene interrogation in a complex microbiome

Cell. 2022 Feb 3;185(3):547-562.e22. doi: 10.1016/j.cell.2021.12.035. Epub 2022 Jan 19.

Abstract

Hundreds of microbiota genes are associated with host biology/disease. Unraveling the causal contribution of a microbiota gene to host biology remains difficult because many are encoded by nonmodel gut commensals and not genetically targetable. A general approach to identify their gene transfer methodology and build their gene manipulation tools would enable mechanistic dissections of their impact on host physiology. We developed a pipeline that identifies the gene transfer methods for multiple nonmodel microbes spanning five phyla, and we demonstrated the utility of their genetic tools by modulating microbiome-derived short-chain fatty acids and bile acids in vitro and in the host. In a proof-of-principle study, by deleting a commensal gene for bile acid synthesis in a complex microbiome, we discovered an intriguing role of this gene in regulating colon inflammation. This technology will enable genetically engineering the nonmodel gut microbiome and facilitate mechanistic dissection of microbiota-host interactions.

Keywords: Firmicutes/Clostridia; bile acid metabolism; colitis; complex gut microbiome; genetic manipulation tools; host-microbe interactions; nonmodel gut microbes.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bile Acids and Salts / metabolism
  • CRISPR-Cas Systems / genetics
  • Clostridium / genetics
  • Colitis / chemically induced
  • Colitis / microbiology
  • Colitis / pathology
  • Dextran Sulfate
  • Drug Resistance, Microbial / genetics
  • Female
  • Gastrointestinal Microbiome / genetics*
  • Gene Expression Regulation, Bacterial
  • Gene Transfer Techniques
  • Genes, Bacterial*
  • Germ-Free Life
  • Inflammation / pathology
  • Intestines / pathology
  • Male
  • Metabolome / genetics
  • Metagenomics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutagenesis, Insertional / genetics
  • Mutation / genetics
  • RNA, Ribosomal, 16S / genetics
  • Transcription, Genetic

Substances

  • Bile Acids and Salts
  • RNA, Ribosomal, 16S
  • Dextran Sulfate