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PhoR1-PhoP1, a third two-component system of the family PhoRP from Myxococcus xanthus: role in development.

ABSTRACT: The pair PhoR1-PhoP1 is the third two-component system of the family PhoRP reported in M. xanthus. PhoR1 is a histidine kinase anchored to the membrane through a transmembrane domain located in the amino-terminal portion of the protein. As a result, 93% of the protein is located in the cytoplasm. This topology is unusual in the PhoR-type histidine kinases. PhoP1 is a response regulator with a helix-loop-helix motif typical of the DNA-binding proteins. Although the operon phoPR1 is expressed during vegetative growth, it peaks during development. The expression levels of this operon are higher in phosphate-containing media than in those in which the nutrient is absent. A deletion mutant in this system exhibits a delay in aggregation and the formation of fruiting bodies larger than those of the wild-type strain. The expression of the operon is autoregulated. This system is also partially responsible for the expression of Mg-independent acid and neutral phosphatases, but it is not required for the expression of alkaline phosphatases.

SUBMITTER: Carrero-Lerida J

PROVIDER: S-EPMC1169532 | biostudies-literature | 2005 Jul

REPOSITORIES: biostudies-literature

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PhoR1-PhoP1, a third two-component system of the family PhoRP from Myxococcus xanthus: role in development.

Carrero-Lérida Juana J Moraleda-Muñoz Aurelio A García-Hernández Raquel R Pérez Juana J Muñoz-Dorado José J

Journal of bacteriology 20050701 14

The pair PhoR1-PhoP1 is the third two-component system of the family PhoRP reported in M. xanthus. PhoR1 is a histidine kinase anchored to the membrane through a transmembrane domain located in the amino-terminal portion of the protein. As a result, 93% of the protein is located in the cytoplasm. This topology is unusual in the PhoR-type histidine kinases. PhoP1 is a response regulator with a helix-loop-helix motif typical of the DNA-binding proteins. Although the operon phoPR1 is expressed duri ...[more]

PMID: 15995213

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Project description:Myxococcus xanthus serves as a model organism for development and complex signal transduction. Regulation of developmental aggregation and sporulation is controlled, in part, by the Che3 chemosensory system. The Che3 pathway consists of homologs to two methyl-accepting chemotaxis proteins (MCPs), CheA, CheW, CheB, and CheR but not CheY. Instead, the output for Che3 is the NtrC homolog CrdA, which functions to regulate developmental gene expression. In this paper we have identified an additional kinase, CrdS, which directly regulates the phosphorylation state of CrdA. Both epistasis and in vitro phosphotransfer assays indicate that CrdS functions as part of the Che3 pathway and, in addition to CheA3, serves to regulate CrdA phosphorylation in M. xanthus. We provide kinetic data for CrdS autophosphorylation and demonstrate specificity for phosphotransfer from CrdS to CrdA. We further demonstrate that CheA3 destabilizes phosphorylated CrdA (CrdA~P), indicating that CheA3 likely acts as a phosphatase. Both CrdS and CheA3 control developmental progression by regulating the phosphorylation state of CrdA~P in the cell. These results support a model in which a classical two-component system and a chemosensory system act synergistically to control the activity of the response regulator CrdA. IMPORTANCE While phosphorylation-mediated signal transduction is well understood in prototypical chemotaxis and two-component systems (TCS), chemosensory regulation of alternative cellular functions (ACF) has not been clearly defined. The Che3 system in Myxococcus xanthus is a member of the ACF class of chemosensory systems and regulates development via the transcription factor CrdA (chemosensory regulator of development) (K. Wuichet and I. B. Zhulin, Sci. Signal. 3:ra50, 2010; J. R. Kirby and D. R. Zusman, Proc. Natl. Acad. Sci. U. S. A. 100:2008-2013, 2003). We have identified and characterized a homolog of NtrB, designated CrdS, capable of specifically phosphorylating the NtrC homolog CrdA in M. xanthus. Additionally, we demonstrate that the CrdSA two-component system is negatively regulated by CheA3, the central processor within the Che3 system of M. xanthus. To our knowledge, this study provides the first example of an ACF chemosensory system regulating a prototypical two-component system and extends our understanding of complex regulation of developmental signaling pathways.

Project description:UNLABELLED:Myxococcus xanthus produces several extracellular signals that guide fruiting body morphogenesis and spore differentiation. Mutants defective in producing a signal may be rescued by codevelopment with wild-type cells or cell fractions containing the signal. In this paper, we identify two molecules that rescue development of the E signal-deficient mutant LS1191 at physiological concentrations, iso15:0 branched-chain fatty acid (FA) and 1-iso15:0-alkyl-2,3-di-iso15:0-acyl glycerol (TG1), a development-specific monoalkyl-diacylglycerol. The physiological concentrations of the bioactive lipids were determined by mass spectrometry from developing wild-type cells using chemically synthesized standards. Synthetic TG1 restored fruiting body morphogenesis and sporulation and activated the expression of the developmentally regulated gene with locus tag MXAN_2146 at physiological concentrations, unlike its nearly identical tri-iso15:0 triacylglycerol (TAG) counterpart, which has an ester linkage instead of an ether linkage. iso15:0 FA restored development at physiological concentrations, unlike palmitic acid, a straight-chain fatty acid. The addition of either lipid stimulates cell shortening, with an 87% decline in membrane surface area, concomitantly with the production of lipid bodies at each cell pole and in the center of the cell. We suggest that cells produce triacylglycerol from membrane phospholipids. Bioactive lipids may be released by programmed cell death (PCD), which claims up to 80% of developing cells, since cells undergoing PCD produce lipid bodies before lysing. IMPORTANCE:Like mammalian adipose tissue, many of the M. xanthus lipid body lipids are triacylglycerols (TAGs), containing ester-linked fatty acids. In both systems, ester-linked fatty acids are retrieved from TAGs with lipases and consumed by the fatty acid degradation cycle. Both mammals and M. xanthus also produce lipids containing ether-linked fatty alcohols with alkyl or vinyl linkages, such as plasmalogens. Alkyl and vinyl linkages are not hydrolyzed by lipases, and no clear role has emerged for lipids bearing them. For example, plasmalogen deficiency in mice has detrimental consequences to spermatocyte development, myelination, axonal survival, eye development, and long-term survival, though the precise reasons remain elusive. Lipids containing alkyl- and vinyl-linked fatty alcohols are development-specific products in M. xanthus. Here, we show that one of them rescues the development of E signal-producing mutants at physiological concentrations.

Dataset Information

PhoR1-PhoP1, a third two-component system of the family PhoRP from Myxococcus xanthus: role in development.

Publications

PhoR1-PhoP1, a third two-component system of the family PhoRP from Myxococcus xanthus: role in development.

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