A Ribose-Scavenging System Confers Colonization Fitness on the Human Gut Symbiont Bacteroides thetaiotaomicron in a Diet-Specific Manner

Cell Host Microbe. 2020 Jan 8;27(1):79-92.e9. doi: 10.1016/j.chom.2019.11.009. Epub 2019 Dec 31.

Abstract

Efficient nutrient acquisition in the human gut is essential for microbial persistence. Although polysaccharides have been well-studied nutrients for the gut microbiome, other resources such as nucleic acids and nucleosides are less studied. We describe several ribose-utilization systems (RUSs) that are broadly represented in Bacteroidetes and appear to have diversified to access ribose from a variety of substrates. One Bacteroides thetaiotaomicron RUS variant is critical for competitive gut colonization in a diet-specific fashion. We used molecular genetics to probe the required functions of the system and the nature of the nutrient source(s) underlying this phenotype. Two RUS-encoded ribokinases were the only components required for this effect, presumably because they generate ribose-phosphate derivatives from products of an unlinked but essential nucleoside phosphorylase. Our results underscore the extensive mechanisms that gut symbionts have evolved to access nutrients and the potential for unexpected dependencies among systems that mediate colonization and persistence.

Keywords: Bacteroides; microbiome; microbiota; nucleoside; ribokinase; ribose; symbiont.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bacteroides thetaiotaomicron* / genetics
  • Bacteroides thetaiotaomicron* / metabolism
  • Diet
  • Gastrointestinal Microbiome / genetics
  • Gene Expression Regulation, Bacterial
  • Genes, Bacterial
  • Mice
  • Pentosyltransferases / genetics*
  • Pentosyltransferases / metabolism
  • Phosphotransferases (Alcohol Group Acceptor) / genetics*
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Ribose / metabolism*
  • Symbiosis

Substances

  • Ribose
  • Pentosyltransferases
  • nucleoside phosphorylase
  • Phosphotransferases (Alcohol Group Acceptor)
  • ribokinase