LOV Histidine Kinase Modulates the General Stress Response System and Affects the virB Operon Expression in Brucella abortus

Sycz, Gabriela; Carrica, Mariela Carmen; Tseng, Tong-Seung; Bogomolni, Roberto A.; Briggs, Winslow R.; Goldbaum, Fernando A.; París, Gastón

doi:10.1371/journal.pone.0124058

Cited by 25 publications

(23 citation statements)

References 63 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Alternatively, arm-in-arm BRR dimers may provide a cooperative mechanism for signal transduction by doubling the local concentration of phosphoacceptor sites. This mechanism might increase the efficiency of an RR that acts as a phosphate sink in a multicomponent TCS to fine-tune signaling, as has been proposed for the LovR RR in the blue light-regulated LOV HK pathway (53,54). A molecular picture of how BRRs couple light sensing by BphPs to phenotypic responses is the next major knowledge gap to be addressed.…”

Section: Rtbrrmentioning

confidence: 99%

Arm-in-Arm Response Regulator Dimers Promote Intermolecular Signal Transduction

et al. 2016

View full text Add to dashboard Cite

Bacteriophytochrome photoreceptors (BphPs) and their cognate response regulators make up two-component signal transduction systems which direct bacteria to mount phenotypic responses to changes in environmental light quality. Most of these systems utilize single-domain response regulators to transduce signals through unknown pathways and mechanisms. Here we describe the photocycle and autophosphorylation kinetics of RtBphP1, a red light-regulated histidine kinase from the desert bacterium Ramlibacter tataouinensis. RtBphP1 undergoes red to far-red photoconversion with rapid thermal reversion to the dark state. RtBphP1 is autophosphorylated in the dark; this activity is inhibited under red light. The RtBphP1 cognate response regulator, the R. tataouinensis bacteriophytochrome response regulator (RtBRR), and a homolog, AtBRR from Agrobacterium tumefaciens, crystallize unexpectedly as arm-in-arm dimers, reliant on a conserved hydrophobic motif, hFWAhL (where h is a hydrophobic M, V, L, or I residue). RtBRR and AtBRR dimerize distinctly from four structurally characterized phytochrome response regulators found in photosynthetic organisms and from all other receiver domain homodimers in the Protein Data Bank. A unique cacodylate-zinc-histidine tag metal organic framework yielded single-wavelength anomalous diffraction phases and may be of general interest. Examination of the effect of the BRR stoichiometry on signal transduction showed that phosphorylated RtBRR is accumulated more efficiently than the engineered monomeric RtBRR (RtBRR mon ) in phosphotransfer reactions. Thus, we conclude that arm-in-arm dimers are a relevant signaling intermediate in this class of two-component regulatory systems. IMPORTANCEBphP histidine kinases and their cognate response regulators comprise widespread red light-sensing two-component systems. Much work on BphPs has focused on structural understanding of light sensing and on enhancing the natural infrared fluorescence of these proteins, rather than on signal transduction or the resultant phenotypes. To begin to address this knowledge gap, we solved the crystal structures of two single-domain response regulators encoded by a region immediately downstream of that encoding BphPs. We observed a previously unknown arm-in-arm dimer linkage. Monomerization via deletion of the C-terminal dimerization motif had an inhibitory effect on net response regulator phosphorylation, underlining the importance of these unusual dimers for signal transduction. Bacteria utilize two-component systems (TCSs) to monitor and respond to diverse signals in the environment, including the spectrum and intensity of visible (Vis) light. Light of a specific wavelength can control directed responses, as in the case of phototaxis (1, 2), or can control generalized stress responses (3). Bacteriophytochrome photoreceptors (BphPs) are soluble cytoplasmic red light-sensing modules, often histidine kinases (HKs), encoded by a region adjacent to a single-domain response regulator (SDRR) to which phosphate is transfe...

show abstract

Section: Rtbrrmentioning

confidence: 99%

Arm-in-Arm Response Regulator Dimers Promote Intermolecular Signal Transduction

et al. 2016

View full text Add to dashboard Cite

show abstract

“…Staron and Mascher [34] noted that genomes containing PhyR and EcfG also contain HWE/HisKA2 kinases, and suggested this family of kinases as candidate regulators of GSR. Indeed, all histidine kinases demonstrated to phosphorylate PhyR and/or regulate GSR transcription to date are HWE/HisKA2 kinases [7,9–11,36–40]. The only histidine kinase known to signal to the GSR pathway that is not HWE/HisKA2 does so indirectly via an HWE/HisKA2 kinase that directly phosphorylates PhyR [9,41].…”

Section: Phylogenetic Distribution and Functionmentioning

confidence: 99%

Structure and function of HWE/HisKA2-family sensor histidine kinases

Herrou

Crosson

Fiebig

2017

Current Opinion in Microbiology

View full text Add to dashboard Cite

Sensor histidine kinases regulate adaptive cellular responses to changes in the chemical or physical state of the environment. HWE/HisKA2-family kinases comprise a subset of histidine kinases that is defined by unique sequence motifs in both the catalytic and non-catalytic regions. Recent crystal structures have defined conserved intramolecular interactions that inform models of kinase regulation that are unique to the HWE/HisKA2 superfamily. Emerging genetic, biochemical and genomic data indicate that, unlike typical histidine kinases, HWE/HisKA2 kinases do not generally signal via classical DNA-binding response regulators. Rather, these unusual kinases are often part of atypical regulatory pathways that control changes in gene expression via modulation of protein-protein interactions or transcription anti-termination.

show abstract

“…B. abortus encodes an extracytoplasmic functiontype sigma factor, σ E1 , which directly and indirectly regulates transcription of approximately 100 genes in response to environmental perturbation. σ E1 -dependent transcription confers resistance to multiple environmental stressors and is required for maintenance of chronic B. abortus infection in a mouse model (4)(5)(6)(7). Assigning physiological and/or biochemical functions to σ E1 -regulated genes is therefore important for understanding B. abortus stress physiology and infection biology.…”

Section: Introductionmentioning

confidence: 99%