Identification of Allobaculum mucolyticum as a novel human intestinal mucin degrader

Gut Microbes. 2021 Jan-Dec;13(1):1966278. doi: 10.1080/19490976.2021.1966278.

Abstract

The human gut microbiota plays a central role in intestinal health and disease. Yet, many of its bacterial constituents are functionally still largely unexplored. A crucial prerequisite for bacterial survival and proliferation is the creation and/or exploitation of an own niche. For many bacterial species that are linked to human disease, the inner mucus layer was found to be an important niche. Allobaculum mucolyticum is a newly identified, IBD-associated species that is thought be closely associated with the host epithelium. To explore how this bacterium is able to effectively colonize this niche, we screened its genome for factors that may contribute to mucosal colonization. Up to 60 genes encoding putative Carbohydrate Active Enzymes (CAZymes) were identified in the genome of A. mucolyticum. Mass spectrometry revealed 49 CAZymes of which 26 were significantly enriched in its secretome. Functional assays demonstrated the presence of CAZyme activity in A. mucolyticum conditioned medium, degradation of human mucin O-glycans, and utilization of liberated non-terminal monosaccharides for bacterial growth. The results support a model in which sialidases and fucosidases remove terminal O-glycan sugars enabling subsequent degradation and utilization of carbohydrates for A. mucolyticum growth. A. mucolyticum CAZyme secretion may thus facilitate bacterial colonization and degradation of the mucus layer and may pose an interesting target for future therapeutic intervention.

Keywords: Allobaculum mucolyticum; cazymes; glycosidase; intestinal mucin; microbiota; mucin degradation; mucin o-glycans; pathobiont; proteome.

MeSH terms

  • Colitis, Ulcerative / microbiology
  • Colitis, Ulcerative / pathology
  • Firmicutes / classification
  • Firmicutes / genetics
  • Firmicutes / metabolism*
  • Gastrointestinal Microbiome / physiology
  • Genome, Bacterial / genetics
  • Humans
  • Intestinal Mucosa / microbiology*
  • Intestinal Mucosa / pathology*
  • Intestines / metabolism
  • Intestines / microbiology
  • Mucins / metabolism*
  • Neuraminidase / metabolism
  • alpha-L-Fucosidase / metabolism

Substances

  • Mucins
  • Neuraminidase
  • alpha-L-Fucosidase