Journal Article

Ruminococcus torques is a keystone degrader of intestinal mucin glycoprotein, releasing oligosaccharides used by Bacteroides thetaiotaomicron

Göteborgs Universitet = University of Gothenburg (GU), Madlambayan, Emily, Architecture et fonction des macromolécules biologiques (AFMB) ; Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Jin, Chunsheng, Luis, Ana, Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia, Martens, Eric, Vasconcelos Pereira, Gabriel, Henrissat, Bernard, Schaus, Sadie, Ostrowski, Matthew, Department of Microbiology and Immunology, University of Michigan Medical School ; University of Michigan [Ann Arbor] ; University of Michigan System-University of Michigan System, Centre Interdisciplinaire de Nanoscience de Marseille (CINaM) ; Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Hansson, Gunnar, University of Michigan [Ann Arbor] ; University of Michigan System, Terrapon, Nicolas

2024

Overview

ABSTRACT Symbiotic interactions between humans and our communities of resident gut microbes (microbiota) play many roles in health and disease. Some gut bacteria utilize mucus as a nutrient source and can under certain conditions damage the protective barrier it forms, increasing disease susceptibility. We investigated how Ruminococcus torques— a known mucin degrader that has been implicated in inflammatory bowel diseases (IBDs)—degrades mucin glycoproteins or their component O -linked glycans to understand its effects on the availability of mucin-derived nutrients for other bacteria. We found that R. torques utilizes both mucin glycoproteins and released oligosaccharides from gastric and colonic mucins, degrading these substrates with a panoply of mostly constitutively expressed, secreted enzymes. Investigation of mucin oligosaccharide degradation by R. torques revealed strong α-L-fucosidase, sialidase and β1,4-galactosidase activities. There was a lack of detectable sulfatase and weak β1,3-galactosidase degradation, resulting in accumulation of glycans containing these structures on mucin polypeptides. While the Gram-negative symbiont, Bacteroides thetaiotaomicron grows poorly on mucin glycoproteins, we demonstrate a clear ability of R. torques to liberate products from mucins, making them accessible to B. thetaiotaomicron . This work underscores the diversity of mucin-degrading mechanisms in different bacterial species and the probability that some species are contingent on others for the ability to more fully access mucin-derived nutrients. The ability of R. torques to directly degrade a variety of mucin and mucin glycan structures and unlock released glycans for other species suggests that it is a keystone mucin degrader, which might contribute to its association with IBD. IMPORTANCE An important facet of maintaining healthy symbiosis between host and intestinal microbes is the mucus layer, the first defense protecting the epithelium from lumenal bacteria. Some gut bacteria degrade the various components of intestinal mucins, but detailed mechanisms used by different species are still emerging. It is imperative to understand these mechanisms as they likely dictate interspecies interactions and may illuminate species associated with bacterial mucus damage and subsequent disease susceptibility. Ruminococcus torques is positively associated with IBD in multiple studies. We identified mucin glycan-degrading enzymes in R. torques and found that it shares mucin degradation products with another species of gut bacteria, Bacteroides thetaiotaomicron . Our findings underscore the importance of understanding mucin degradation mechanisms in different gut bacteria and their consequences on interspecies interactions, which may identify keystone bacteria that disproportionately affect mucus damage and could therefore be key players in effects that result from reductions in mucus integrity.

• Publisher: American Society for Microbiology,CCSD
• Subject: Bacteria / Bacteroides thetaiotaomicron / Biodegradation / Blood groups / Crohn's disease / Degradation products / Digestive system / Enzymes / Epithelium / Fatty acids / Gastrointestinal Microbiome / Gastrointestinal tract / Glucose / glycoprotein / Glycoproteins / Human Microbiome / Humans / inflammatory bowel disease / Inflammatory bowel diseases / Intestine / Life Sciences / Microbiology in the Medical Area / microbiota / Microorganisms / Mikrobiologi inom det medicinska området / Molecular weight / Mucin / Mucins / Mucus / Nutrients / Oligosaccharides / Polysaccharides / Research Article / Ruminococcus / Ruminococcus torques / Species / Symbiosis
• ISBN: 0012651653000