Reciprocal Prioritization to Dietary Glycans by Gut Bacteria in a Competitive Environment Promotes Stable Coexistence

Abstract

When presented with nutrient mixtures, several human gut Bacteroides species exhibit hierarchical utilization of glycans through a phenomenon that resembles catabolite repression. However, it is unclear how closely these observed physiological changes, often measured by altered transcription of glycan utilization genes, mirror actual glycan depletion. To understand the glycan prioritization strategies of two closely related human gut symbionts, Bacteroides ovatus and Bacteroides thetaiotaomicron, we performed a series of time course assays in which both species were individually grown in a medium with six different glycans that both species can degrade. Disappearance of the substrates and transcription of the corresponding polysaccharide utilization loci (PULs) were measured. Each species utilized some glycans before others, but with different priorities per species, providing insight into species-specific hierarchical preferences. In general, the presence of highly prioritized glycans repressed transcription of genes involved in utilizing lower-priority nutrients. However, transcriptional sensitivity to some glycans varied relative to the residual concentration in the medium, with some PULs that target high-priority substrates remaining highly expressed even after their target glycan had been mostly depleted. Coculturing of these organisms in the same mixture showed that the hierarchical orders generally remained the same, promoting stable coexistence. Polymer length was found to be a contributing factor for glycan utilization, thereby affecting its place in the hierarchy. Our findings not only elucidate how B. ovatus and B. thetaiotaomicron strategically access glycans to maintain coexistence but also support the prioritization of carbohydrate utilization based on carbohydrate structure, advancing our understanding of the relationships between diet and the gut microbiome.

Multiple stable states in microbial communities explained by the stable marriage problem

“…The competitive interactions summarized in these tables are just starting to be explored experimentally. In fact, the first experimental results relevant to communities within the human gut have already been reported [61,54]. Specifically, these results demonstrate the preferences and competitive abilities of 2 Bacteroides species for 9 particular polysaccharides.…”

“…Recent work by Martens and collaborators [61,55,40] has established that many species in Bacteroides (the most prevalent genus in the human gut microbiome [51,12]) exhibit this kind of preferential nutrient utilization -with respect to polysaccharides present in a typical diet [20]. Interestingly, even species such as B. ovatus and B. thetaiotaomicron -which are closely-related evolutionarily -display rather different polysaccharide preference hierarchies [61].…”

Facilitation promotes invasions in plant‐associated microbial communities

“…2016). For example, previous studies have demonstrated that bacteria can show diet preference between different dietary glycans, which can prolong species coexistence in co-cultures (Tuncil et al 2017). Such dietary preference might leave some resources less utilised, providing an opportunity for invasion (Tilman 1999).…”

Cross-feeding interactions of gut symbionts driven by human milk oligosaccharidesand mucins

“…The glycan-foraging capability could enhance the bacterial fitness and colonisation in the infant gut (Martens et al 2008) and the finestructure prioritisation at species level has been accounted for the collective fitness of Bacteroides spp. (Tuncil et al 2017). As such, several HMOS structures including 2'-FL, LNFP I, and LDFT were found to correlate positively with the abundance of Bacteroides spp.…”