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Open Access Research article

Acid shock of Listeria monocytogenes at low environmental temperatures induces prfA, epithelial cell invasion, and lethality towards Caenorhabditis elegans

Klaus Neuhaus1, Peter Satorhelyi12, Kristina Schauer3, Siegfried Scherer1 and Thilo M Fuchs1*

Author Affiliations

1 Lehrstuhl für Mikrobielle Ökologie, Department für biowissenschaftliche Grundlagen, Wissenschaftszentrum Weihenstephan, and ZIEL, Abteilung Mikrobiologie, Technische Universität München, Weihenstephaner Berg 3, Freising, 85350, Germany

2 Present Address: IVAX Drug Research Institute, Berlini u. 49, Budapest, 1045, Hungary

3 Present Address: Lehrstuhl für Hygiene und Technologie der Milch, Tiermedizinische Fakultät der Ludwig-Maximilians-Universität München, Schönleutnerstrasse 8, Oberschleißheim, D-85764, Germany

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BMC Genomics 2013, 14:285  doi:10.1186/1471-2164-14-285

Published: 27 April 2013

Abstract

Background

The saprophytic pathogen Listeria monocytogenes has to cope with a variety of acidic habitats during its life cycle. The impact of low-temperature coupled with pH decrease for global gene expression and subsequent virulence properties, however, has not been elucidated.

Results

qRT-PCR revealed for the first time a transient, acid triggered prfA induction of approximately 4-fold, 5.7-fold, 7-fold and 9.3-fold 60 to 90 min after acid shock of L. monocytogenes at 37°C, 25°C, 18°C, and 10°C, respectively. Comparable data were obtained for seven different L. monocytogenes strains, demonstrating that prfA induction under these conditions is a general response of L. monocytogenes. Transcriptome analysis revealed that the in vivo-relevant genes bsh, clpP, glpD, hfq, inlA, inlB, inlE, lisR, and lplA1 as well as many other genes with a putative role during infection are transiently induced upon acid shock conducted at 25°C and 37°C. Twenty-five genes repressed upon acid shock are known to be down regulated during intracellular growth or by virulence regulators. These data were confirmed by qRT-PCR of twelve differentially regulated genes and by the identification of acid shock-induced genes influenced by σB. To test if up regulation of virulence genes at temperatures below 37°C correlates with pathogenicity, the capacity of L. monocytogenes to invade epithelial cells after acid shock at 25°C was measured. A 12-fold increased number of intracellular bacteria was observed (acid shock, t = 60 min) that was reduced after adaptation to the level of the unshocked control. This increased invasiveness was shown to be in line with the induction of inlAB. Using a nematode infection assay, we demonstrated that Caenorhabditis elegans fed with acid-shocked L. monocytogenes exhibits a shorter time to death of 50% (TD50) of the worms (6.4 days) compared to infection with unshocked bacteria (TD50 = 10.2 days).

Conclusions

PrfA and other listerial virulence genes are induced by an inorganic acid in a temperature-dependent manner. The data presented here suggest that low pH serves as a trigger for listerial pathogenicity at environmental temperatures.

Keywords:
Listeria monocytogenes; Virulence genes; Acidic pH; prfA; Invertebrates; Transcriptome; Global response; Invasion