Blue and Red Light Modulates SigB-Dependent Gene Transcription, Swimming Motility and Invasiveness in Listeria monocytogenes

Nicolai Ondrusch,Jürgen Kreft

doi:10.1371/journal.pone.0016151

Abstract

BackgroundIn a number of gram-positive bacteria, including Listeria, the general stress response is regulated by the alternative sigma factor B (SigB). Common stressors which lead to the activation of SigB and the SigB-dependent regulon are high osmolarity, acid and several more. Recently is has been shown that also blue and red light activates SigB in Bacillus subtilis.Methodology/Principal FindingsBy qRT-PCR we analyzed the transcriptional response of the pathogen L. monocytogenes to blue and red light in wild type bacteria and in isogenic deletion mutants for the putative blue-light receptor Lmo0799 and the stress sigma factor SigB. It was found that both blue (455 nm) and red (625 nm) light induced the transcription of sigB and SigB-dependent genes, this induction was completely abolished in the SigB mutant. The blue-light effect was largely dependent on Lmo0799, proving that this protein is a genuine blue-light receptor. The deletion of lmo0799 enhanced the red-light effect, the underlying mechanism as well as that of SigB activation by red light remains unknown. Blue light led to an increased transcription of the internalin A/B genes and of bacterial invasiveness for Caco-2 enterocytes. Exposure to blue light also strongly inhibited swimming motility of the bacteria in a Lmo0799- and SigB-dependent manner, red light had no effect there.Conclusions/SignificanceOur data established that visible, in particular blue light is an important environmental signal with an impact on gene expression and physiology of the non-phototrophic bacterium L. monocytogenes. In natural environments these effects will result in sometimes random but potentially also cyclic fluctuations of gene activity, depending on the light conditions prevailing in the respective habitat.

Highlights

The genus comprises eight species, L. monocytogenes and L. ivanovii are pathogenic for humans and/or animals, L. seeligeri is considered as nonvirulent, L. innocua, L. welshimeri, L. grayi, L. marthii and L. rocourtiae are harmless saprophytes
Lmo0799 of Listeria monocytogenes EGD-e is highly similar to YtvA from Bacillus subtilis, homologues are present in all sequenced L. monocytogenes isolates and in other Listeria species
During a recent investigation into the thiol:disulfide redox metabolism of Listeria monocytogenes EGD-e we observed that, together with the genes for thioredoxin A and thioredoxin reductase, the transcription of lmo0799 was highly up regulated when the bacteria were selectively depleted for the biological thiol glutathione (GSH) by a deletion in the glutathione synthetase gene gshF

Summary

Introduction

Listeriosis, a systemic disease caused in humans by L. monocytogenes, is rare but has a high mortality in severe manifestations, e.g. sepsis and meningoencephalitis. It turned out that pathogenic Listeriae contain a chromosomal cluster of genes (Vcl) which are essential for virulence. The products of these virulence genes are involved in the escape of Listeria from the phagosome of the host cell, in actinbased intracellular movement of the bacteria and in their spreading to neighbouring cells [5,8,9]. In a number of gram-positive bacteria, including Listeria, the general stress response is regulated by the alternative sigma factor B (SigB). Is has been shown that blue and red light activates SigB in Bacillus subtilis

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