Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins.

Abstract

We previously reported that the oligosaccharide chains of hog gastric mucin were degraded by unidentified subpopulations numbering 1% of normal human fecal bacteria. Here we report on the enzyme-producing properties of five strains of mucin oligosaccharide chain-degrading bacteria isolated from feces of four healthy subjects. Four were isolated from the greatest fecal dilutions yielding mucin side chain-degrading activity in culture, and thus were the numerically dominant side chain-degrading bacteria in their respective hosts. Three were Ruminococcus strains and two were Bifidobacterium strains. Two Ruminococcus torques strains, IX-70 and VIII-239, produced blood group A-and H-degrading a-glycosidase activities, sialidase, and the requisite jl-glycosidases; these strains released >90% of the anthrone-reacting hexoses from hog gastric mucin during growth in culture. The Bifidobacterium strains lacked A-degrading activity but were otherwise similar, these released 60-80% of the anthrone-reacting hexoses but not the A antigenic structures from hog gastric mucin. Only Ruminococcus AB strain VI-268 produced blood group B-degrading a-galactosidase activity, but this strain lacked ,5-N-acetyl exosaminidases to complete degradation of B antigenic chains. When this strain was co-cultured with a strain that produced jl-N-acetylhexosaminidases, release of hexoses from blood group B salivary glycoprotein increased from 50 to >90%, and bacterial growth was enhanced. The glycosidases required for side chain degradation were produced by these strains in the absence of mucin substrate, and a substantial fraction of each activity in stationary phase cultures was extracellular. In contrast, none of 16 other fecal Bacteroides, Escherichia coli, Streptococcus faecalis, and Bifidobacterium strains produced ABH blood group-degrading enzymes; other glycosidases produced by these strains were predominantly cell bound except for extracellular j-N-acetylhexosaminidases produced by the five S. faecalis strains.We conclude that certain Bifidobacterium and Ruminococcus strains are numerically dominant populations degrading mucin oligosaccharides in the human colon due to their constitutive production of the requisite extracellular glycosidases including blood group antigen-specific a-glycosidases. These properties characterize them as a functionally distinct subpopulation of normal human enteric microflora comprised of An abstract of portions of this work was published in Gastroenterology 1983; 84:1191.

Carbon nutrition of Escherichia coli in the mouse intestine

“…The hypothesis is oversimplified if considered from the perspective that each of the 500 species present grows best on a single simple nutrient; there simply are not that many nutrients available in the ecosystem. Instead, it seems prudent to consider that the complex microbial community of the intestine is established by competition for diverse nutrients that are generated in the intestine through mucosal polysaccharide degradation to release free sugars and distinct oligosaccharides with various carbohydrate compositions (10).…”

“…Most carbohydrate in the colon is in the form of mucosal polysaccharides, which are degraded by a few anaerobes that dominate the intestinal biota (9)(10)(11). The monosaccharides released from mucin and other mucosal glycoproteins support the growth of many intestinal bacteria such as E. coli, which does not make polysaccharide-degrading enzymes (10).…”

“…Most carbohydrate in the colon is in the form of mucosal polysaccharides, which are degraded by a few anaerobes that dominate the intestinal biota (9)(10)(11). The monosaccharides released from mucin and other mucosal glycoproteins support the growth of many intestinal bacteria such as E. coli, which does not make polysaccharide-degrading enzymes (10). Because the population of individual species is proportional to the concentration of its preferred nutrient(s), the relatively low population of E. coli in the intestine indicates that the concentration of its preferred nutrient(s) is low.…”

Modulation of intestinal mucin composition and mucosal morphology by dietary phytogenic inclusion level in broilers

“…Furthermore the changes in mucin monosaccharide composition pattern as in Gal, Fuc and GalNac molar ratios need to be further assessed in terms of overall gut microbial ecology, as it is known that a correlation between mucin composition and bacterial colonization and proliferation exits. The latter is evidenced via the degradation of mucin by bacterial glycosidases (Hoskins et al, 1986;Ruas-Madiedo et al, 2008), the bacterial utilization of mucin carbohydrate side chains as energy source (Salyers, 1979;Scwad and Gä nzle, 2011;Stahl et al, 2011) and the bacterial adhesion in mucin monosaccharide (Kirjavainen et al, 1998;Gusils et al, 2003), as well as the ability of gut microflora to modulate intestinal glycosylation (Bry et al, 1996;Gheri Bryk et al, 1999;Freitas et al, 2005) and mucin gene expression (Mack et al, 1999 and. Therefore, this correlation may determine to a significant extent which species or even strains within species are best suited for utilization, colonization and/or adhesion to intestinal mucus.…”

“…Mucin monosaccharide composition depends on a dynamic interaction between adhesion of intestinal bacteria (Kirjavainen et al, 1998;Ouwehand et al, 1999;Gusils et al, 2003), host intestinal glycosylation (Bry et al, 1996;Gheri Bryk et al, 1999;Freitas et al, 2005) and microbial degradation by the intestinal microflora (Hoskins et al, 1986;Ruas-Madiedo et al, 2008).…”