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Global gene regulation in Yersinia enterocolitica: effect of FliA on the expression levels of flagellar and plasmid-encoded virulence genes

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Abstract

This study describes the involvement of the sigma factor of the flagellar system, FliA, in global gene regulation of Yersinia enterocolitica. In addition to exhibiting a positive effect upon the expression levels of eight class III flagellar operons, FliA also exhibited a negative effect upon the expression levels of four virulence operons that are located on the pYV virulence plasmid. These are yadA, virC, yopQ, and the insertion element ISYen1. While the positive effect on class III flagellar operons by FliA is most likely direct, the negative effect on the virulence operons appears to require the known transcriptional activator of these genes, VirF. This was determined using microarray analysis, quantitative PCR and a search for putative binding sites for FliA. In addition to the FliA regulation of flagellar and plasmid-encoded virulence genes, we studied temperature regulation of these genes. While wild-type cells exhibited increased expression levels of flagellar genes and decreased expression levels of plasmid-encoded virulence genes at 25°C (as compared to 37°C), temperature dependence of gene expression was much reduced in the fliA mutants. We conclude that FliA contributes to the inverse temperature regulation of flagellar and plasmid-encoded virulence genes. We present a network of transcriptional regulation around FlhD/FlhC and FliA.

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Abbreviations

ORF:

Open reading frame

PCR:

Polymerase chain reaction

PMT:

Photomultiplier tube

QPCR:

Quantitative PCR

YOP:

Yersinia outer proteins

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Acknowledgments

The authors would like to thank Dr. Philip Matsumura (University of Illinois, Chicago, IL, USA) for providing microarray slides, Dr. Scott A. Minnich (University of Idaho, Moscow, ID, USA) for providing strains, Dr. Phillip McClean (North Dakota State University, Fargo, ND, USA) for allowing us to use his microarray scanner, Sheri Dorsam, Rian Lee, Megan Townsend, and Jody Englin (North Dakota State University, Fargo, ND, USA) for technical assistance with various aspects of this project, and Dr. Charlene Wolf-Hall, Dr. Catherine Logue, and Dr. Eugene Berry (North Dakota State University, Fargo, ND, USA) for critically reading the manuscript. In addition, we thank the anonymous reviewers that contributed greatly to this manuscript. The research was supported by the BRIN and ND EPSCoR (through NSF grant #EPS-0132289) programs of North Dakota, the NDSU Agricultural Experiment Station, and the ‘Biosecurity, Disease Surveillance, and Food Safety’ earmark grant (through USDA-APHIS). The authors also thank the researchers at the Sanger Institute for providing their annotation data through their website.

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  1. Department of Veterinary and Microbiological Sciences, North Dakota State University, 1523 Centennial Blvd., Fargo, ND, 58105, USA

    Shelley M. Horne & Birgit M. Prüß

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Correspondence to Birgit M. Prüß.

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Horne, S.M., Prüß, B.M. Global gene regulation in Yersinia enterocolitica: effect of FliA on the expression levels of flagellar and plasmid-encoded virulence genes. Arch Microbiol 185, 115–126 (2006). https://doi.org/10.1007/s00203-005-0077-1

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