Abstract
The food-borne pathogen Listeria monocytogenes encodes two chitinases, ChiA and ChiB, which allow the bacterium to hydrolyze chitin, the second most abundant polysaccharide in nature. Intriguingly, despite the absence of chitin in human and mammalian hosts, both of the chitinases have been deemed important for infection, through a mechanism that, at least in the case of ChiA, involves modulation of host immune responses. In this study, we show that the expression of the two chitinases is subject to regulation by the listerial agr system, a homologue of the agr quorum-sensing system of Staphylococcus aureus, that has so far been implicated in virulence and biofilm formation. We demonstrate that in addition to these roles, the listerial agr system is required for efficient chitin hydrolysis, as deletion of agrD, encoding the putative precursor of the agr autoinducer, dramatically decreased chitinolytic activity on agar plates. Agr was specifically induced in response to chitin addition in stationary phase and agrD was found to regulate the amount of chiA, but not chiB, transcripts. Although the transcript levels of chiB did not depend on agrD, the extracellular protein levels of both chitinases were reduced in the ΔagrD mutant. The regulatory effect of agr on chiA is potentially mediated through the small RNA LhrA, which we show here to be negatively regulated by agr. LhrA is in turn known to repress chiA translation by binding to the chiA transcript and interfering with ribosome recruitment. Our results highlight a previously unrecognized role of the agr system and suggest that autoinducer-based regulation of chitinolytic systems may be more commonplace than previously thought.
Highlights
IntroductionL. monocytogenes is often isolated from marine environments, as well as from soil, where it lives as a saprophyte [1,2,3]
Listeria monocytogenes is a Gram-positive food-borne pathogen, and the causative agent of human listeriosis, a disease of varying severity that can prove fatal for immunosusceptible patient groups, such as pregnant women and the elderly.L. monocytogenes is often isolated from marine environments, as well as from soil, where it lives as a saprophyte [1,2,3]
A DagrD mutant is impaired in chitin hydrolysis In L. monocytogenes agrD is predicted to encode the premature form of the autoinducing peptide of the agr system [26,33]
Summary
L. monocytogenes is often isolated from marine environments, as well as from soil, where it lives as a saprophyte [1,2,3]. In these habitats, chitin, a polymer of N-acetylglucosamine (GlcNAc) and the second most abundant carbohydrate in nature, can constitute an important source of carbon and nitrogen [4,5,6,7,8]. Many bacteria autochthonous to chitin-rich environments have developed simple to complex chitinolytic systems, which allow them to degrade chitin and use it as a nutrient source [4,8,9]. Many human and animal pathogens are chitinolytic, and evidence has emerged that chitinases and LMPOs have an additional key role in these pathogens as virulence factors, which promote infection [12]
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