Prioritization of polysaccharide utilization and control of regulator activation inBacteroides thetaiotaomicron

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Abstract

Summary

Bacteroides thetaiotaomicron is a human gut symbiotic bacterium that utilizes a myriad of host dietary and mucosal polysaccharides. The proteins responsible for the uptake and breakdown of many of these polysaccharides are transcriptionally regulated by hybrid two-component systems (HTCSs). These systems consist of a single polypeptide harboring the domains of sensor kinases and response regulators, and thus, are thought to autophosphorylate in response to specific signals. We now report that the HTCS BT0366 is phosphorylated in vivo when B. thetaiotaomicron experiences the BT0366 inducer arabinan but not when grown in the presence of glucose. BT0366 phosphorylation and transcription of BT0366-activated genes requires the conserved predicted sites of phosphorylation in BT0366. When chondroitin sulfate is added to arabinan-containing cultures, BT0366 phosphorylation and transcription of BT0366-activated genes are inhibited and the bacterium exhibits diauxic growth. Whereas 20 additional combinations of polysaccharides also give rise to diauxic growth, other combinations result in synergistic or unaltered growth relative to bacteria experiencing a single polysaccharide. The different strategies employed by B. thetaiotaomicron when faced with multiple polysaccharides may aid its competitiveness in the mammalian gut.

Bacteroides thetaiotaomicron exhibits variable growth phenotypes when exposed to distinct pairs of polysaccharides. Activation of hybrid two-component systems, which promote transcription of polysaccharide utilization genes, requires phosphorylation at conserved residues. Certain polysaccharides inhibit activation of hybrid two-component systems necessary for non-preferred polysaccharide breakdown, which results in polysaccharide preference and growth diauxie.

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