Bacteroides thetaiotaomicron enhances H2S production in Bilophila wadsworthia

Gut Microbes. 2024 Jan-Dec;16(1):2431644. doi: 10.1080/19490976.2024.2431644. Epub 2024 Nov 28.

Abstract

Sulfate- and sulfite-reducing bacteria (SRB) are a group of strict anaerobes found within the human gut. Bilophila wadsworthia, a sulfite-reducing bacterium which produces hydrogen sulfide (H2S) from taurine and isethionate respiration, is a common member of the healthy commensal human gut microbiota but has been implicated in several disease states including inflammatory bowel disease and colorectal cancer. Bacteroides thetaiotaomicron, one of the most prominent gut bacteria, has sulfatases which release sulfate, serving as a potential substrate for sulfate-reducing bacteria. Here, we showed that when B. thetaiotaomicron and B. wadsworthia were in co-culture, there was a significant increase in B. thetaiotaomicron's growth and in H2S production by B. wadsworthia. Differential gene expression analysis revealed increased expression of B. wadsworthia's dsrMKJOP complex in co-culture, which delivers electrons for sulfite reduction to H2S. This was accompanied by a decreased expression of genes associated with taurine, sulfolactate, and thiosulfate respiration, indicating that B. thetaiotaomicron may provide an alternative source of sulfite to B. wadsworthia. We hypothesized adenosine 5'-phosphosulfate (APS) to be this intermediate. Indeed, B. wadsworthia was able to grow using APS or sulfite as electron acceptors. Endometabolomic and transcriptomic analyses revealed decreased production of indole by B. thetaiotaomicron in co-culture with B. wadsworthia due to enhanced tryptophan utilization by B. wadsworthia. The results of this microbe-microbe interaction could have significant pro-inflammatory effects in the human gut environment.

Keywords: Sulfite-reducing bacteria; adenosine 5’-phosphosulfate; hydrogen sulfide; indole.

MeSH terms

  • Bacteroides thetaiotaomicron* / enzymology
  • Bacteroides thetaiotaomicron* / genetics
  • Bacteroides thetaiotaomicron* / metabolism
  • Bilophila* / genetics
  • Bilophila* / metabolism
  • Coculture Techniques
  • Gastrointestinal Microbiome*
  • Humans
  • Hydrogen Sulfide* / metabolism
  • Sulfates / metabolism
  • Sulfites / metabolism
  • Taurine / metabolism

Substances

  • Hydrogen Sulfide
  • Taurine
  • Sulfites
  • Sulfates

Grants and funding

This work was supported by UKRI-BBSRC via the Norwich Research Park Doctoral Training Partnership [grant no. BB/M011216/1] and institute strategic programme grants Gut Microbes and Health [BB/R012490/1 theme BBS/E/F/000PR10356] and Food, Microbiome and Health (BB/X011054/1 theme BBS/E/F/000PR13633). UKRI-BBSRC had no role in the manner of conduct or outcome of the research project. Transcriptomic sequencing was funded through a Quadram Institute Bioscience Institute Development Grant [20414000X]. LS was supported by a BBSRC Discovery Fellowship [BB/Z514445/10].