Comparative analysis of LytS/LytTR-type histidine kinase/response regulator systems in γ-proteobacteria

Bacterial histidine kinase/response regulator systems operate at the interface between environmental cues and physiological states. Escherichia coli contains two LytS/LytTR-type histidine kinase/response regulator systems, BtsS/BtsR (formerly YehU/YehT) and YpdA/YpdB, which have been identified as pyruvate-responsive two-component systems. Since they exhibit remarkable similarity, we analyzed their phylogenetic distribution within the γ-proteobacteria, and experimentally characterized them in a set of representative species. We found that BtsS/BtsR is the predominant LytS/LytTR-type two-component system among γ-proteobacteria, whereas YpdA/YpdB primarily appears in a supplementary role. Based on our observations in E. coli, we used the highly conserved DNA-binding motifs to test the in vivo functionality of both systems in various genera, including Salmonella, Enterobacter, Citrobacter, Xenorhabdus, Yersinia, Aeromonas and Vibrio. The results suggest that, in all cases tested, BtsS/BtsR and YpdA/YpdB respond to different levels of pyruvate in the environment.

[1]  R. Bandyopadhyay,et al.  Study of dynamical heterogeneities in colloidal nanoclay suspensions approaching dynamical arrest , 2017, Scientific Reports.

[2]  K. Jung,et al.  Identification of a High-Affinity Pyruvate Receptor in Escherichia coli , 2017, Scientific Reports.

[3]  R. Heermann,et al.  Insights into the DNA-binding mechanism of a LytTR-type transcription regulator , 2016, Bioscience reports.

[4]  Robert D. Finn,et al.  The Pfam protein families database: towards a more sustainable future , 2015, Nucleic Acids Res..

[5]  S. Mazmanian,et al.  Gut biogeography of the bacterial microbiota , 2015, Nature Reviews Microbiology.

[6]  V. Appanna,et al.  Glycine metabolism and anti-oxidative defence mechanisms in Pseudomonas fluorescens. , 2015, Microbiological research.

[7]  K. Jung,et al.  Identification of a Novel Nutrient-Sensing Histidine Kinase/Response Regulator Network in Escherichia coli , 2014, Journal of bacteriology.

[8]  X. F. Yang,et al.  Pyruvate Protects Pathogenic Spirochetes from H2O2 Killing , 2014, PloS one.

[9]  Andrew J. Page,et al.  Characterization of the yehUT Two-Component Regulatory System of Salmonella enterica Serovar Typhi and Typhimurium , 2013, PloS one.

[10]  Kirsten Jung,et al.  Identification of a Target Gene and Activating Stimulus for the YpdA/YpdB Histidine Kinase/Response Regulator System in Escherichia coli , 2012, Journal of bacteriology.

[11]  K. Jung,et al.  First Insights into the Unexplored Two-Component System YehU/YehT in Escherichia coli , 2012, Journal of bacteriology.

[12]  J. Asara,et al.  A positive/negative ion–switching, targeted mass spectrometry–based metabolomics platform for bodily fluids, cells, and fresh and fixed tissue , 2012, Nature Protocols.

[13]  Kirsten Jung,et al.  Histidine kinases and response regulators in networks. , 2012, Current opinion in microbiology.

[14]  Reinhard Guthke,et al.  More than just a metabolic regulator - elucidation and validation of new targets of PdhR in Escherichia coli , 2011, BMC Systems Biology.

[15]  N. Barkai,et al.  The Competitive Advantage of a Dual-Transporter System , 2011, Science.

[16]  S. Hultgren,et al.  A central metabolic circuit controlled by QseC in pathogenic Escherichia coli , 2011, Molecular microbiology.

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

[18]  F. Thompson,et al.  Comparative genomic analyses identify the Vibrio harveyi genome sequenced strains BAA-1116 and HY01 as Vibrio campbellii , 2009, Environmental microbiology reports.

[19]  C. Alteri,et al.  Fitness of Escherichia coli during Urinary Tract Infection Requires Gluconeogenesis and the TCA Cycle , 2009, PLoS pathogens.

[20]  D. Sidote,et al.  Structure of the Staphylococcus aureus AgrA LytTR domain bound to DNA reveals a beta fold with an unusual mode of binding. , 2008, Structure.

[21]  Michael Y. Galperin.  Telling bacteria: do not LytTR. , 2008, Structure.

[22]  J. Raser,et al.  Positive feedback regulates switching of phosphate transporters in S. cerevisiae. , 2007, Molecular cell.

[23]  Uwe Sauer,et al.  The PEP-pyruvate-oxaloacetate node as the switch point for carbon flux distribution in bacteria. , 2005, FEMS microbiology reviews.

[24]  P. Hogeweg,et al.  The alignment of sets of sequences and the construction of phyletic trees: An integrated method , 2005, Journal of Molecular Evolution.

[25]  R. Zoraghi,et al.  Properties and functions of GAF domains in cyclic nucleotide phosphodiesterases and other proteins. , 2004, Molecular pharmacology.

[26]  Nikolaus Rajewsky,et al.  The evolution of DNA regulatory regions for proteo-gamma bacteria by interspecies comparisons. , 2002, Genome research.

[27]  J. Stock,et al.  The histidine protein kinase superfamily. , 1999, Advances in microbial physiology.

[28]  Gapped BLAST and PSI-BLAST: A new , 1997 .

[29]  S. Jeffery.  Evolution of Protein Molecules , 1979 .