Abstract

Bifidobacteria resident in the gastrointestinal tract (GIT) are subject to constantly changing environmental conditions, which require rapid adjustments in gene expression. Here, we show that two predicted LacI-type transcription factors (TFs), designated AraQ and MalR1, are involved in regulating the central, carbohydrate-associated metabolic pathway (the so-called phosphoketolase pathway or bifid shunt) of the gut commensal Bifidobacterium breve UCC2003. These TFs appear to not only control transcription of genes involved in the bifid shunt and each other, but also seem to commonly and directly affect transcription of other TF-encoding genes, as well as genes related to uptake and metabolism of various carbohydrates. This complex and interactive network of AraQ/MalR1-mediated gene regulation provides previously unknown insights into the governance of carbon metabolism in bifidobacteria.

Highlights

  • The microbial communities within the human gastrointestinal tract (GIT), commonly referred to as the gut microbiota, have enjoyed intense scientific scrutiny and are predominantly made up of members of the bacterial phyla Bacteroidetes, Firmicutes, Proteobacteria and Actinobacteria[1,2]

  • We show here that two of the previously identified LacI-type transcription factors (TFs) appear to be directly involved in transcriptionally regulating genetic components of the bifid shunt, as well as genes involved in a range of specific carbohydrate metabolic pathways, thereby revealing a previously undiscovered global carbohydrate control network, which is predicted to operate in many bifidobacterial species

  • The distal gut does not supply bacteria with a reliable carbon source; available carbohydrates are dependent on many factors such as host diet and other bacteria present in the GIT

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Summary

Introduction

The microbial communities within the human gastrointestinal tract (GIT), commonly referred to as the gut microbiota, have enjoyed intense scientific scrutiny and are predominantly made up of members of the bacterial phyla Bacteroidetes, Firmicutes, Proteobacteria and Actinobacteria[1,2]. 8–15% of the bifidobacterial coding capacity is dedicated to carbohydrate uptake and metabolism, depending on species and functional gene assignment[16,17] These estimates are consistent with the well-documented ability of bifidobacteria to utilise a diverse array of carbohydrates[16,18]. Phylogenetic and protein modelling studies have recently suggested that the bifidobacterial XFPK enzyme is related to that found in members of the Coriobacteriales order and that xfpK was horizontally transferred between (an ancestor of) these two groups[21,28,29] Another interesting difference between bifidobacteria (and possibly Coriobacteriales) and other bacteria is that they lack a number of enzymes, such as phosphofructokinase, which are crucial to control central carbohydrate metabolism[30]. We show here that two of the previously identified LacI-type TFs appear to be directly involved in transcriptionally regulating genetic components of the bifid shunt, as well as genes involved in a range of specific carbohydrate metabolic pathways, thereby revealing a previously undiscovered global carbohydrate control network, which is predicted to operate in many bifidobacterial species

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