Phenotypic and genomic diversification in complex carbohydrate degrading human gut bacteria

Abstract

Symbiotic bacteria are responsible for the majority of complex carbohydrate digestion in the human colon. Since the identities and amounts of dietary polysaccharides directly impact the gut microbiota, determining which microorganisms consume specific nutrients is central to defining the relationship between diet and gut microbial ecology. Using a custom phenotyping array, we determined carbohydrate utilization profiles for 354 members of the Bacteroidetes, a dominant saccharolytic phylum. There was wide variation in the numbers and types of substrates degraded by individual bacteria, but phenotype-based clustering grouped members of the same species indicating that each species performs characteristic roles. The ability to utilize dietary polysaccharides and endogenous mucin glycans was negatively correlated, suggesting exclusion between these niches. By analyzing related Bacteroides ovatus/xylanisolvens strains that vary in their ability to utilize mucin glycans, we addressed whether gene clusters that confer this complex, multi-locus trait are being gained or lost in individual strains. Pangenome reconstruction of these strains revealed a remarkably mosaic architecture in which genes involved in polysaccharide metabolism are highly variable and bioinformatics data provide evidence of interspecies gene transfer that might explain this genomic heterogeneity. Global transcriptomic analyses suggest that the ability to utilize mucin has been lost in some lineages of B. ovatus and B. xylanisolvens, which still harbor residual gene clusters that are involved in mucin utilization by strains that still actively express this phenotype. Our data provide insight into the breadth and complexity of carbohydrate metabolism in the microbiome and the underlying genomic events that shape these behaviors.

Origins and Evolution of NovelBacteroidesin Captive Apes

“…For example, one upregulated gene, that encoding sialate O-acetylesterase, removes mucin side groups, which enables cross-species foraging of mucin by pathogenic bacteria (Robinson et al 2017). Additionally, ß-galactosidase, which shows a 150-fold increase in expression (Pudlo et al 2021), is also known to be important in mucin degradation (Tsilford et al 2015; Bell and Juge 2021).…”

“…Acquisition of these new genes or loss of these genes by XB1A may indicate that some B. xylanisolvens strains can grow on colonic mucin; however, testing this is complicated by the fact that colonic mucin, unlike gastric mucin, is not readily available (Luis et al 2020). Due to the wide variation in carbohydrate metabolism among closely related strains and the dependence on substrates related to particular host species and/or diet [78, 79], caution must be applied to narratives about the metabolic capabilities of a bacterial species based on few isolates (Pudlo et al 2021; Luis et al 2020; de Paepe et al, 2018).…”

“…Recent work has demonstrated that individual Bacteroides species tend to specialize in degrading either host-derived or dietary-derived polysaccharides, suggesting that species can co-exist because they occupy distinct functional niches [10]. In contrast to other Bacteroides species, Bacteroides xylanisolvens strains exhibit extreme variation in the ability to metabolize host mucin and plant-derived polysaccharides (Lewis et al 2020; Hao et al 2021; Pudlo et al 2021). Moreover, these functional differences are evident among strains that are otherwise identical by ribosomal RNA profiling (Pudlo et al 2021).…”

“…In contrast to other Bacteroides species, Bacteroides xylanisolvens strains exhibit extreme variation in the ability to metabolize host mucin and plant-derived polysaccharides (Lewis et al 2020; Hao et al 2021; Pudlo et al 2021). Moreover, these functional differences are evident among strains that are otherwise identical by ribosomal RNA profiling (Pudlo et al 2021).…”

Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus

“…Using a defined microbial community of five species, another group found that B. ovatus increased in growth with pectin ( Liu et al, 2020 ). Work by Pudlo et al (2021) identified that multiple B. ovatus strains could use pectins, starch, fructans, and glycosaminoglycans. These findings, as well as our own, indicate that the addition of polysaccharides like inulin and pectin to the diet could promote B. ovatus growth and potentially increase B. ovatus levels in the colon.…”