Expression of Signal Transduction System Encoding Genes of Yersinia pseudotuberculosis IP32953 at 28°C and 3°C

Yersinia pseudotuberculosis is a significant psychrotrophic food pathogen whose cold tolerance mechanisms are poorly understood. Signal transduction systems serve to monitor the environment, but no systematic investigation of their role at cold temperatures in Y. pseudotuberculosis has yet been undertaken. The relative expression levels of 54 genes predicted to encode proteins belonging to signal transduction systems in Y. pseudotuberculosis IP32953 were determined at 28°C and 3°C by quantitative real-time reverse transcription-PCR. The relative expression levels of 44 genes were significantly (p<0.05) higher at 3°C than at 28°C. Genes encoding the two-component system CheA/CheY had the highest relative expression levels at 3°C. Mutational analysis revealed that cheA is important for growth and motility at 3°C. The relative expression level of one gene, rssB, encoding an RpoS regulator, was significantly (p<0.05) lower at 3°C than at 28°C. The results suggest that several signal transduction systems might be used during growth at low temperature, and at least, CheA/CheY two-component system is important for low-temperature growth.

[1]  R. E. Black,et al.  Yersinia enterocolitica. , 2022, Infectious disease clinics of North America.

[2]  B. Görke,et al.  Common and divergent features in transcriptional control of the homologous small RNAs GlmY and GlmZ in Enterobacteriaceae , 2010, Nucleic acids research.

[3]  J. Bielecki,et al.  OmpR controls Yersinia enterocolitica motility by positive regulation of flhDC expression , 2010, Antonie van Leeuwenhoek.

[4]  I. Dahiya,et al.  Yersinia ruckeri genes that attenuate survival in rainbow trout (Oncorhynchus mykiss) are identified using signature-tagged mutants. , 2010, Veterinary microbiology.

[5]  I. Dahiya,et al.  The UvrY response regulator of the BarA–UvrY two-component system contributes to Yersinia ruckeri infection of rainbow trout (Oncorhynchus mykiss) , 2010, Archives of Microbiology.

[6]  R. Bourret,et al.  Two-component signal transduction. , 2010, Current opinion in microbiology.

[7]  Eveliina Palonen,et al.  Adaptation of enteropathogenic Yersinia to low growth temperature , 2010, Critical reviews in microbiology.

[8]  S. Minnich,et al.  Yersinia pestis Two-Component Gene Regulatory Systems Promote Survival in Human Neutrophils , 2009, Infection and Immunity.

[9]  Shiyun Chen,et al.  Positive regulation of flhDC expression by OmpR in Yersinia pseudotuberculosis. , 2009, Microbiology.

[10]  R. Hengge Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. , 2009, Research in microbiology.

[11]  Shiyun Chen,et al.  OmpR positively regulates urease expression to enhance acid survival of Yersinia pseudotuberculosis. , 2009, Microbiology.

[12]  Christopher A. Voigt,et al.  Kinetic buffering of cross talk between bacterial two-component sensors. , 2009, Journal of molecular biology.

[13]  B. Shutinoski,et al.  Controlled activation of the Cpx system is essential for growth of Yersinia enterocolitica. , 2009, FEMS microbiology letters.

[14]  Astrid Oust Janbu,et al.  Global responses of Escherichia coli to adverse conditions determined by microarrays and FT-IR spectroscopy. , 2009, Canadian journal of microbiology.

[15]  Shiyun Chen,et al.  Functional characterization of FlgM in the regulation of flagellar synthesis and motility in Yersinia pseudotuberculosis. , 2009, Microbiology.

[16]  D. Clarke,et al.  Comparative functional analysis of the RcsC sensor kinase from different Enterobacteriaceae. , 2009, FEMS microbiology letters.

[17]  Robert D. Finn,et al.  InterPro: the integrative protein signature database , 2008, Nucleic Acids Res..

[18]  P. Williams,et al.  Functional interplay between the Yersinia pseudotuberculosis YpsRI and YtbRI quorum sensing systems modulates swimming motility by controlling expression of flhDC and fliA , 2008, Molecular microbiology.

[19]  B. J. Hinnebusch,et al.  Experimental evidence for negative selection in the evolution of a Yersinia pestis pseudogene , 2008, Proceedings of the National Academy of Sciences.

[20]  M. Rohde,et al.  A Csr‐type regulatory system, including small non‐coding RNAs, regulates the global virulence regulator RovA of Yersinia pseudotuberculosis through RovM , 2008, Molecular microbiology.

[21]  B. Wren,et al.  The importance of the Rcs phosphorelay in the survival and pathogenesis of the enteropathogenic yersiniae. , 2008, Microbiology.

[22]  I. Ricard,et al.  Phenotypic analysis of Yersinia pseudotuberculosis 32777 response regulator mutants: new insights into two-component system regulon plasticity in bacteria. , 2008, International journal of medical microbiology : IJMM.

[23]  Ruifu Yang,et al.  Identification and characterization of PhoP regulon members in Yersinia pestis biovar Microtus , 2008, BMC Genomics.

[24]  A. Siitonen,et al.  Yersinia pseudotuberculosis causing a large outbreak associated with carrots in Finland, 2006 , 2008, Epidemiology and Infection.

[25]  M. Laub,et al.  Specificity in two-component signal transduction pathways. , 2007, Annual review of genetics.

[26]  Shiyun Chen,et al.  The flhDC gene affects motility and biofilm formation in Yersinia pseudotuberculosis , 2007, Science in China Series C: Life Sciences.

[27]  M. Wiedmann,et al.  Microarray-Based Characterization of the Listeria monocytogenes Cold Regulon in Log- and Stationary-Phase Cells , 2007, Applied and Environmental Microbiology.

[28]  I. Bukowska,et al.  OmpR negatively regulates expression of invasin in Yersinia enterocolitica. , 2007, Microbiology.

[29]  Katrin E. Carlsson,et al.  Influence of the Cpx Extracytoplasmic-Stress-Responsive Pathway on Yersinia sp.-Eukaryotic Cell Contact , 2007, Infection and Immunity.

[30]  Katrin E. Carlsson,et al.  Extracytoplasmic-Stress-Responsive Pathways Modulate Type III Secretion in Yersinia pseudotuberculosis , 2007, Infection and Immunity.

[31]  R. Stephan,et al.  Evaluation of housekeeping genes in Listeria monocytogenes as potential internal control references for normalizing mRNA expression levels in stress adaptation models using real-time PCR. , 2007, FEMS microbiology letters.

[32]  A. Siitonen,et al.  An outbreak of gastrointestinal illness and erythema nodosum from grated carrots contaminated with Yersinia pseudotuberculosis. , 2006, The Journal of infectious diseases.

[33]  J. Mecsas,et al.  Intranasal Inoculation of Mice with Yersinia pseudotuberculosis Causes a Lethal Lung Infection That Is Dependent on Yersinia Outer Proteins andPhoP , 2006, Infection and Immunity.

[34]  J. Bliska,et al.  Characterization of Phagosome Trafficking and Identification of PhoP-Regulated Genes Important for Survival of Yersinia pestis in Macrophages , 2006, Infection and Immunity.

[35]  D. Georgellis,et al.  Signaling by the arc two-component system provides a link between the redox state of the quinone pool and gene expression. , 2006, Antioxidants & redox signaling.

[36]  T. Fuchs,et al.  Transcriptional Analysis of Long-Term Adaptation of Yersinia enterocolitica to Low-Temperature Growth , 2006, Journal of bacteriology.

[37]  S. M. Horne,et al.  Global gene regulation in Yersinia enterocolitica: effect of FliA on the expression levels of flagellar and plasmid-encoded virulence genes , 2006, Archives of Microbiology.

[38]  Regine Hengge,et al.  A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli. , 2005, Genes & development.

[39]  G. Young,et al.  Environmental Regulation and Virulence Attributes of the Ysa Type III Secretion System of Yersinia enterocolitica Biovar 1B , 2005, Infection and Immunity.

[40]  Ruifu Yang,et al.  Transcriptome analysis of the Mg2+-responsive PhoP regulator in Yersinia pestis. , 2005, FEMS microbiology letters.

[41]  M. Marceau Transcriptional regulation in Yersinia: an update. , 2005, Current issues in molecular biology.

[42]  T. Latifi,et al.  Transcriptional Regulation of the 4-Amino-4-deoxy-L-arabinose Biosynthetic Genes in Yersinia pestis* , 2005, Journal of Biological Chemistry.

[43]  R. Utsumi,et al.  Functional Characterization in Vitro of All Two-component Signal Transduction Systems from Escherichia coli* , 2005, Journal of Biological Chemistry.

[44]  B. Lindner,et al.  The pmrF polymyxin-resistance operon of Yersinia pseudotuberculosis is upregulated by the PhoP-PhoQ two-component system but not by PmrA-PmrB, and is not required for virulence. , 2004, Microbiology.

[45]  M. Inouye,et al.  Genome-Wide Transcriptional Analysis of the Cold Shock Response in Wild-Type and Cold-Sensitive, Quadruple-csp-Deletion Strains of Escherichia coli , 2004, Journal of bacteriology.

[46]  J. Bliska,et al.  The Response Regulator PhoP of Yersinia pseudotuberculosis Is Important for Replication in Macrophages and for Virulence , 2004, Infection and Immunity.

[47]  Michelle E. Maxson,et al.  Identification of Inducers of the Yersinia enterocolitica Phage Shock Protein System and Comparison to the Regulation of the RpoE and Cpx Extracytoplasmic Stress Responses , 2004, Journal of bacteriology.

[48]  J. W. Campbell,et al.  Gene array analysis of Yersinia enterocolitica FlhD and FlhC: regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. , 2004, Microbiology.

[49]  Samuel I. Miller,et al.  Variation in lipid A structure in the pathogenic yersiniae , 2004, Molecular microbiology.

[50]  A. Siitonen,et al.  A widespread outbreak of Yersinia pseudotuberculosis O:3 infection from iceberg lettuce. , 2004, The Journal of infectious diseases.

[51]  M. Schmidt,et al.  Regulation of htrA expression in Yersinia enterocolitica. , 2004, FEMS microbiology letters.

[52]  C. Médigue,et al.  Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[53]  A. Zasada,et al.  The osmotic regulator OmpR is involved in the response of Yersinia enterocolitica O:9 to environmental stresses and survival within macrophages. , 2003, FEMS microbiology letters.

[54]  P. Bertin,et al.  Regulation cascade of flagellar expression in Gram-negative bacteria. , 2003, FEMS microbiology reviews.

[55]  B. Wren The Yersiniae — a model genus to study the rapid evolution of bacterial pathogens , 2003, Nature Reviews Microbiology.

[56]  H. Korkeala,et al.  Low Occurrence of Pathogenic Yersinia enterocolitica in Clinical, Food, and Environmental Samples: a Methodological Problem , 2003, Clinical Microbiology Reviews.

[57]  P. Hitchen,et al.  Structural characterization of lipo‐oligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system , 2002, Molecular microbiology.

[58]  E. Winzeler,et al.  Application of High-Density Array-Based Signature-Tagged Mutagenesis To Discover Novel YersiniaVirulence-Associated Genes , 2001, Infection and Immunity.

[59]  M. Pfaffl,et al.  A new mathematical model for relative quantification in real-time RT-PCR. , 2001, Nucleic acids research.

[60]  B. Wren,et al.  The Response Regulator PhoP Is Important for Survival under Conditions of Macrophage-Induced Stress and Virulence in Yersinia pestis , 2000, Infection and Immunity.

[61]  J. Naktin,et al.  Yersinia enterocolitica and Yersinia pseudotuberculosis. , 1999, Clinics in laboratory medicine.

[62]  Michael J. Smith,et al.  The Yersinia enterocolitica Motility Master Regulatory Operon, flhDC, Is Required for Flagellin Production, Swimming Motility, and Swarming Motility , 1999, Journal of bacteriology.

[63]  G. Dougan,et al.  Construction and characterisation of a Yersinia enterocolitica O:8 ompR mutant. , 1998, FEMS microbiology letters.

[64]  V. Kapatral,et al.  Temperature‐dependent regulation of Yersinia enterocolitica Class III flagellar genes , 1996, Molecular microbiology.

[65]  G. Cornelis,et al.  The fliA gene encoding sigma 28 in Yersinia enterocolitica , 1995, Journal of bacteriology.

[66]  M. Surette,et al.  Signal transduction in bacterial chemotaxis , 1992, The Journal of biological chemistry.

[67]  Haruo Watanabe,et al.  Detection and identification of Yersinia pseudotuberculosis and pathogenic Yersinia enterocolitica by an improved polymerase chain reaction method , 1992, Journal of clinical microbiology.

[68]  É. Carniel,et al.  A highly efficient electroporation system for transformation of Yersinia. , 1990, Gene.

[69]  M. Gomyoda,et al.  Cat-contaminated environmental substances lead to Yersinia pseudotuberculosis infection in children , 1989, Journal of clinical microbiology.

[70]  in chief George M. Garrity Bergey’s Manual® of Systematic Bacteriology , 1989, Springer New York.

[71]  N. Saunders,et al.  Rapid extraction of bacterial genomic DNA with guanidium thiocyanate , 1989 .

[72]  M. Gomyoda,et al.  Yersinia pseudotuberculosis infection contracted through water contaminated by a wild animal , 1988, Journal of clinical microbiology.

[73]  G. Garrity Bergey’s Manual® of Systematic Bacteriology , 2012, Springer New York.

[74]  A. Koumoutsi,et al.  The response regulator PhoP negatively regulates Yersinia pseudotuberculosis and Yersinia pestis biofilms. , 2009, FEMS microbiology letters.

[75]  J. Sofos,et al.  Pathogens and toxins in foods : challenges and interventions , 2009 .

[76]  T. Tobe The roles of two-component systems in virulence of pathogenic Escherichia coli and Shigella spp. , 2008, Advances in experimental medicine and biology.

[77]  K. Brzostek,et al.  The YompC protein ofYersinia enterocolitica: Molecular and physiological characterization , 2008, Folia Microbiologica.

[78]  T. Fuchs,et al.  Presence of a functional flagellar cluster Flag-2 and low-temperature expression of flagellar genes in Yersinia enterocolitica W22703. , 2008, Microbiology.

[79]  J. Gowrishankar,et al.  Th1-type immune response to infection by pYV-cured phoP-phoQ null mutant of Yersinia pseudotuberculosis is defective in mouse model , 2008, Antonie van Leeuwenhoek.

[80]  Abby L. Berns,et al.  Low temperature (23 degrees C) increases expression of biofilm-, cold-shock- and RpoS-dependent genes in Escherichia coli K-12. , 2008, Microbiology.

[81]  I. Ricard,et al.  Two-component system regulon plasticity in bacteria: a concept emerging from phenotypic analysis of Yersinia pseudotuberculosis response regulator mutants. , 2007, Advances in experimental medicine and biology.

[82]  K. Brzostek,et al.  Identification of OmpR protein and its role in the invasion properties of Yersinia enterocolitica. , 2004, Polish journal of microbiology.

[83]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[84]  S. Kaneko,et al.  Detection of pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis from pork using the polymerase chain reaction. , 1995, Contributions to microbiology and immunology.

[85]  G. Cornelis,et al.  The fliA Gene Encoding s in Yersinia enterocolitica , 1995 .