Ruminococcus gnavus: friend or foe for human health

Abstract

Ruminococcus gnavus was first identified in 1974 as a strict anaerobe in the gut of healthy individuals, and for several decades, its study has been limited to specific enzymes or bacteriocins. With the advent of metagenomics, R. gnavus has been associated both positively and negatively with an increasing number of intestinal and extraintestinal diseases from inflammatory bowel diseases to neurological disorders. This prompted renewed interest in understanding the adaptation mechanisms of R. gnavus to the gut, and the molecular mediators affecting its association with health and disease. From ca. 250 publications citing R. gnavus since 1990, 94% were published in the last 10 years. In this review, we describe the biological characterization of R. gnavus, its occurrence in the infant and adult gut microbiota and the factors influencing its colonization of the gastrointestinal tract; we also discuss the current state of our knowledge on its role in host health and disease. We highlight gaps in knowledge and discuss the hypothesis that differential health outcomes associated with R. gnavus in the gut are strain and niche specific.

Keywords: Ruminococcus gnavus; carbohydrate metabolism; gut adaptation; intestinal and extraintestinal diseases; metabolites; mucus.

Figure 1.

Scanning electron microscopy image of R. gnavus ATCC 35913 anaerobically grown in rich medium to stationary phase (courtesy of Catherine Booth).

Figure 2.

Distribution of GHs across R. gnavus strains. A total of 7741 putative GHs has been identified by analysing 92 genomes of R. gnavus strains. These GHs are spread across 56 GH families. Some GH families are not widely spread amongst R. gnavus strains (i.e. GH35, GH38, GH53, GH65, GH79, GH84, GH91, GH101, GH120, GH125, and GH154) while other families are present in all the strains (i.e. GH1, GH2, GH3, GH13, GH18, GH25, GH29, GH31, GH32, GH36, GH73, GH77, GH78, GH95, GH112, and GH151). More than half of the sequences (4021/7741) belongs to seven GH families: GH1, GH2, GH3, GH13, GH23, GH32, and GH73. Combined, these families cover enzymes with a wide range of activities including (but not exclusively) α-amylase, isoamylase, pullulanase, β-glucosidase, β-galactosidase, β-mannosidase, β-glucuronidase, β-xylosidase, lysozyme, peptidoglycan hydrolase, invertase, inulinase, and endo-levanase.

Figure 3.

R. gnavus association in diseases and potential molecular mediators.