Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB

Terán-Melo, Juan Luis; Peña-Sandoval, Gabriela R.; Silva-Jiménez, Hortencia; Rodríguez, Claudia; Álvarez, Adrián F.; Georgellis, Dimitris

doi:10.1074/jbc.ra118.003910

Cited by 20 publications

(22 citation statements)

References 46 publications

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“…S2C in the supplemental material), indicating that AccS is a bifunctional enzyme that possesses both kinase and phosphatase activities. This observation is in agreement with previous knowledge that SKs normally have two enzymatic activities, an autophosphorylation (kinase) activity and, in the unphosphorylated state, a phosphatase activity, that together determine the phosphorylation state of their cognate response regulator (4, 39, 51, 52).…”

Section: Discussionsupporting

confidence: 93%

A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in Azoarcus sp. CIB

Valderrama

Gómez-Álvarez

Martín‐Moldes

et al. 2019

mBio

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We have identified and characterized the AccS multidomain sensor kinase that mediates the activation of the AccR master regulator involved in carbon catabolite repression (CCR) of the anaerobic catabolism of aromatic compounds inAzoarcussp. CIB. A truncated AccS protein that contains only the soluble C-terminal autokinase module (AccS′) accounts for the succinate-dependent CCR control. In vitroassays with purified AccS′ revealed its autophosphorylation, phosphotransfer from AccS′∼P to the Asp60 residue of AccR, and the phosphatase activity toward its phosphorylated response regulator, indicating that the equilibrium between the kinase and phosphatase activities of AccS′ may control the phosphorylation state of the AccR transcriptional regulator. Oxidized quinones, e.g., ubiquinone 0 and menadione, switched the AccS′ autokinase activity off, and three conserved Cys residues, which are not essential for catalysis, are involved in such inhibition. Thiol oxidation by quinones caused a change in the oligomeric state of the AccS′ dimer resulting in the formation of an inactive monomer. This thiol-based redox switch is tuned by the cellular energy state, which can change depending on the carbon source that the cells are using. This work expands the functional diversity of redox-sensitive sensor kinases, showing that they can control new bacterial processes such as CCR of the anaerobic catabolism of aromatic compounds. The AccSR two-component system is conserved in the genomes of some betaproteobacteria, where it might play a more general role in controlling the global metabolic state according to carbon availability.IMPORTANCETwo-component signal transduction systems comprise a sensor histidine kinase and its cognate response regulator, and some have evolved to sense and convert redox signals into regulatory outputs that allow bacteria to adapt to the altered redox environment. The work presented here expands knowledge of the functional diversity of redox-sensing kinases to control carbon catabolite repression (CCR), a phenomenon that allows the selective assimilation of a preferred compound among a mixture of several carbon sources. The newly characterized AccS sensor kinase is responsible for the phosphorylation and activation of the AccR master regulator involved in CCR of the anaerobic degradation of aromatic compounds in the betaproteobacteriumAzoarcussp. CIB. AccS seems to have a thiol-based redox switch that is modulated by the redox state of the quinone pool. The AccSR system is conserved in several betaproteobacteria, where it might play a more general role controlling their global metabolic state.

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Section: Discussionsupporting

confidence: 93%

A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in Azoarcus sp. CIB

Valderrama

Gómez-Álvarez

Martín‐Moldes

et al. 2019

mBio

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“…The phosphoryl group (∼P) is, then, transferred to a conserved aspartate residue at the RD of the cognate RR, rendering it active, often as a transcriptional regulator (1). Some TCSs, however, operate by a more elaborate signal transduction pathway, involving sequential phosphoryl group transfers in a His → Asp → His → Asp multistep phosphorelay (2)(3)(4). Such TCSs comprise hybrid HKs, which contain, in addition to the TD, an RD and a phosphotransfer domain with a conserved histidine residue.…”

mentioning

confidence: 99%

“…In all cases, in the absence of the stimulus, both the RR and the HK dephosphorylate, resulting in silencing of the system. Phosphorylated RR (RR-P) dephosphorylation occurs either by the inherent lability of the mixed anhydride phosphoaspartyl bond and/or by the RR-P−specific phosphatase activity of the cognate HK (4)(5)(6)(7)(8).…”

mentioning

confidence: 99%

Identification of Z nucleotides as an ancient signal for two-component system activation in bacteria

Vázquez-Ciros

Álvarez

Georgellis

2020

Proc. Natl. Acad. Sci. U.S.A.

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Two-component systems (TCSs) in bacteria are molecular circuits that allow the perception of and response to diverse stimuli. These signaling circuits rely on phosphoryl-group transfers between transmitter and receiver domains of sensor kinase and response regulator proteins, and regulate several cellular processes in response to internal or external cues. Phosphorylation, and thereby activation, of response regulators has been demonstrated to occur by their cognate histidine kinases but also by low molecular weight phosphodonors such as acetyl phosphate and carbamoyl phosphate. Here, we present data indicating that the intermediates of the de novo syntheses of purines and histidine, 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranosyl 5′-monophosphate (ZMP) and/or 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranosyl 5′-triphosphate (ZTP), activate the response regulator UvrY, by promoting its autophosphorylation at the conserved aspartate at position 54. Moreover, these Z nucleotides are shown to also activate the nonrelated response regulators ArcA, CpxR, RcsB, and PhoQ. We propose that ZMP and/or ZTP act as alarmones for a wide range of response regulators in vivo, providing a novel mechanism by which they could impact gene expression in response to metabolic cues.

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“…In particular, our finding that a BinK protein containing a REC domain that is locked as non-phosphorylated with the D794A mutation is not only nonfunctional, but is dominant negative as it interferes with signaling of a wild-type binK allele expressed in the same cell. There are published cases in which one monomer’s REC domain interacts with the same monomer’s DHp domain ( in cis ), and other cases in which it interacts with the partner monomer’s DHp domain ( in trans ) (40, 41). In both cases, however, dynamic movement of both monomers is required across the dimer interface (32, 42).…”

Section: Discussionmentioning

confidence: 99%

Hybrid histidine kinase BinK represses Vibrio fischeri biofilm signaling at multiple developmental stages

Ludvik

Bultman

Mandel

2021

Preprint

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The symbiosis between the Hawaiian bobtail squid, Euprymna scolopes, and its exclusive light-organ symbiont, Vibrio fischeri, provides a natural system in which to study host-microbe specificity and gene regulation during the establishment of a mutually-beneficial symbiosis. Colonization of the host relies on bacterial biofilm-like aggregation in the squid mucus field. Symbiotic biofilm formation is controlled by a two-component signaling (TCS) system consisting of regulators RscS-SypF-SypG, which together direct transcription of the Syp symbiotic polysaccharide. TCS systems are broadly important for bacteria to sense environmental cues and then direct changes in behavior. Previously, we identified hybrid histidine kinase BinK as a strong negative regulator of Vibrio fischeri biofilm regulation, and here we further explore the function of BinK. To inhibit biofilm formation, BinK requires the predicted phosphorylation sites in both the histidine kinase (H362) and receiver (D794) domains. Furthermore, we show that a strain lacking BinK yields RscS non-essential for host colonization, and imaging of aggregate size revealed no benefit to the presence of RscS in a background lacking BinK. Strains lacking RscS still suffered in competition, suggesting another function for the protein. Finally, we show that BinK functions to inhibit biofilm gene expression in the light organ crypts, providing evidence for biofilm gene regulation at later stages of host colonization. Overall, this study provides direct evidence for opposing activities of RscS and BinK and yields novel insights into biofilm regulation during the maturation of a beneficial symbiosis.

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Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB

Cited by 20 publications

References 46 publications

A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in Azoarcus sp. CIB

A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in Azoarcus sp. CIB

Identification of Z nucleotides as an ancient signal for two-component system activation in bacteria

Hybrid histidine kinase BinK represses Vibrio fischeri biofilm signaling at multiple developmental stages

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