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Four unusual two-component signal transduction homologs, RedC to RedF, are necessary for timely development in Myxococcus xanthus.

ABSTRACT: We identified a cluster of four two-component signal transduction genes that are necessary for proper progression of Myxococcus xanthus through development. redC to redF mutants developed and sporulated early, resulting in small, numerous, and disorganized fruiting bodies. Yeast two-hybrid analyses suggest that RedCDEF act in a single signaling pathway. The previously identified espA gene displays a phenotype similar to that of redCDEF. However, combined mutants defective in espA redCDEF exhibited a striking additive developmental phenotype, suggesting that EspA and RedC to RedF play independent roles in controlling developmental progression.

SUBMITTER: Higgs PI

PROVIDER: S-EPMC1291262 | biostudies-literature | 2005 Dec

REPOSITORIES: biostudies-literature

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Four unusual two-component signal transduction homologs, RedC to RedF, are necessary for timely development in Myxococcus xanthus.

Higgs Penelope I PI Cho Kyungyun K Whitworth David E DE Evans Lisa S LS Zusman David R DR

Journal of bacteriology 20051201 23

We identified a cluster of four two-component signal transduction genes that are necessary for proper progression of Myxococcus xanthus through development. redC to redF mutants developed and sporulated early, resulting in small, numerous, and disorganized fruiting bodies. Yeast two-hybrid analyses suggest that RedCDEF act in a single signaling pathway. The previously identified espA gene displays a phenotype similar to that of redCDEF. However, combined mutants defective in espA redCDEF exhibit ...[more]

PMID: 16291693

Similar Datasets

A novel "four-component" two-component signal transduction mechanism regulates developmental progression in Myxococcus xanthus.

Project description:Histidine-aspartate phosphorelays are employed by two-component signal transduction family proteins to mediate responses to specific signals or stimuli in microorganisms and plants. The RedCDEF proteins constitute a novel signaling system in which four two-component proteins comprising a histidine kinase, a histidine-kinase like protein, and two response regulators function together to regulate progression through the elaborate developmental program of Myxococcus xanthus. A combination of in vivo phenotypic analyses of in-frame deletions and non-functional point mutations in each gene as well as in vitro autophosphorylation and phosphotransfer analyses of recombinant proteins indicate that the RedC histidine kinase protein autophosphorylates and donates a phosphoryl group to the single domain response regulator, RedF, to repress progression through the developmental program. To relieve this developmental repression, RedC instead phosphorylates RedD, a dual receiver response regulator protein. Surprisingly, RedD transfers the phosphoryl group to the histidine kinase-like protein RedE, which itself appears to be incapable of autophosphorylation. Phosphorylation of RedE may render RedE accessible to RedF, where it removes the phosphoryl group from RedF-P, which is otherwise an unusually stable phosphoprotein. These analyses reveal a novel "four-component" signaling mechanism that has probably arisen to temporally coordinate signals controlling the developmental program in M. xanthus. The RedCDEF signaling system provides an important example of how the inherent plasticity and modularity of the basic two-component signaling domains comprise a highly adaptable framework well suited to expansion into complex signaling mechanisms.

| S-EPMC2755868 | biostudies-other

The Nla28S/Nla28 two-component signal transduction system regulates sporulation in Myxococcus xanthus.

Project description:The response regulator Nla28 is a key component in a cascade of transcriptional activators that modulates expression of many important developmental genes in Myxococcus xanthus. In this study, we identified and characterized Nla28S, a histidine kinase that modulates the activity of this important regulator of M. xanthus developmental genes. We show that the putative cytoplasmic domain of Nla28S has the in vitro biochemical properties of a histidine kinase protein: it hydrolyzes ATP and undergoes an ATP-dependent autophosphorylation that is acid labile and base stable. We also show that the putative cytoplasmic domain of Nla28S transfers a phosphoryl group to Nla28 in vitro, that the phosphotransfer is specific, and that a substitution in the predicted site of Nla28 phosphorylation (aspartate 53) abolishes the phosphotransfer reaction. In phenotypic studies, we found that a mutation in nla28S produces a developmental phenotype similar to, but weaker than, that produced by a mutation in nla28; both mutations primarily affect sporulation. Together, these data indicate that Nla28S is the in vivo histidine kinase partner of Nla28 and that the primary function of the Nla28S/Nla28 two-component signal transduction system is to regulate sporulation genes. The results of genetic studies suggest that phosphorylation of Nla28S is important for the in vivo sporulation function of the Nla28S/Nla28 two-component system. In addition, the quorum signal known as A-signal is important for full developmental expression of the nla28S-nla28 operon, suggesting that quorum signaling regulates the availability of the Nla28S/Nla28 signal transduction circuit in developing cells.

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An adenylyl cyclase, CyaA, of Myxococcus xanthus functions in signal transduction during osmotic stress.

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| S-EPMC135126 | biostudies-literature

Myxococcus xanthus chemotaxis homologs DifD and DifG negatively regulate fibril polysaccharide production.

Project description:The extracellular matrix fibrils of Myxococcus xanthus are essential for the social lifestyle of this unusual bacterium. These fibrils form networks linking or encasing cells and are tightly correlated with cellular cohesion, development, and social (S) gliding motility. Previous studies identified a set of bacterial chemotaxis homologs encoded by the dif locus. It was determined that difA, difC, and difE, encoding respective homologs of a methyl-accepting chemotaxis protein, CheW, and CheA, are required for fibril production and therefore S motility and development. Here we report the studies of three additional genes residing at the dif locus, difB, difD, and difG. difD and difG encode homologs of chemotaxis proteins CheY and CheC, respectively. difB encodes a positively charged protein with limited homology at its N terminus to conserved bacterial proteins with unknown functions. Unlike the previously characterized dif genes, none of these three newly studied dif genes are essential for fibril production, S motility, or development. The difB mutant showed no obvious defects in any of the processes examined. In contrast, the difD and the difG mutants were observed to overproduce fibril polysaccharides in comparison with production by the wild type. The observation that DifD and DifG negatively regulate fibril polysaccharide production strengthens our hypothesis that the M. xanthus dif genes define a chemotaxis-like signal transduction pathway which regulates fibril biogenesis. To our knowledge, this is the first report of functional studies of a CheC homolog in proteobacteria. In addition, during this study, we slightly modified previously developed assays to easily quantify fibril polysaccharide production in M. xanthus.

| S-EPMC344214 | biostudies-literature

The Myxococcus xanthus asgA gene encodes a novel signal transduction protein required for multicellular development.

Project description:The Myxococcus xanthus asgA gene is one of three known genes necessary for the production of extracellular A-signal, a cell density signal required early in fruiting body development. We determined the DNA sequence of asgA. The deduced 385-amino-acid sequence of AsgA was found to contain two domains: one homologous to the receiver domain of response regulators and the other homologous to the transmitter domain of histidine protein kinases. A kanamycin resistance (Kmr) gene was inserted at various positions within or near the asgA gene to determine the null phenotype. Those strains with the Kmr gene inserted upstream or downstream of asgA are able to form fruiting bodies, while strains containing the Kmr gene inserted within asgA fail to develop. The nature and location of the asgA476 mutation were determined. This mutation causes a leucine-to-proline substitution within a conserved stretch of hydrophobic residues in the N-terminal receiver domain. Cells containing the insertion within asgA and cells containing the asgA476 substitution have similar phenotypes with respect to development, colony color, and expression of an asg-dependent gene. An analysis of expression of a translational asgA-lacZ fusion confirms that asgA is expressed during growth and early development. Finally, we propose that AsgA functions within a signal transduction pathway that is required to sense starvation and to respond with the production of extracellular A-signal.

| S-EPMC176844 | biostudies-other

Global profiling of gene expression in A signal mutants of Myxococcus xanthus

Project description:In response to starvation Myxococcus xanthus initiates a developmental program that culminates in the formation of fruiting bodies inside which the rod-shaped cells differentiate to spores. Fruiting body formation depends on intercellular communication and two intercellular signals are known, the A-signal and the C-signal. Five genes have been identified which are required for A-signal synthesis. To begin to understand the function of the genes required for A-signal synthesis, we have analysed gene expression in the asgA and the asgB mutant. Keywords: Vegetative cells of WT (DK1622) and AsgA mutant (DK5057) and AsgB mutant (DK4398)

2012-05-18 | GSE18029 | GEO

Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus.

Project description:Proteins of two-component systems (TCS) have essential functions in the sensing of external and self-generated signals in bacteria and in the generation of appropriate output responses. Accordingly, in Myxococcus xanthus, TCS are important for normal motility and fruiting body formation and sporulation. Here we analyzed the M. xanthus genome for the presence and genetic organization of genes encoding TCS. Two hundred seventy-two TCS genes were identified, 251 of which are not part of che gene clusters. We report that the TCS genes are unusually organized, with 55% being orphan and 16% in complex gene clusters whereas only 29% display the standard paired gene organization. Hybrid histidine protein kinases and histidine protein kinases predicted to be localized to the cytoplasm are overrepresented among proteins encoded by orphan genes or in complex gene clusters. Similarly, response regulators without output domains are overrepresented among proteins encoded by orphan genes or in complex gene clusters. The most frequently occurring output domains in response regulators are involved in DNA binding and cyclic-di-GMP metabolism. Our analyses suggest that TCS encoded by orphan genes and complex gene clusters are functionally distinct from TCS encoded by paired genes and that the connectivity of the pathways made up of TCS encoded by orphan genes and complex gene clusters is different from that of pathways involving TCS encoded by paired genes. Experimentally, we observed that orphan TCS genes are overrepresented among genes that display altered transcription during fruiting body formation. The systematic analysis of the 25 orphan genes encoding histidine protein kinases that are transcriptionally up-regulated during development showed that 2 such genes are likely essential for viability and identified 7 histidine protein kinases, including 4 not previously characterized that have important function in fruiting body formation or spore germination.

| S-EPMC2223698 | biostudies-literature

Global profiling of gene expression in A signal mutants of Myxococcus xanthus

2012-05-17 | E-GEOD-18029 | biostudies-arrayexpress

Transmission of a signal that synchronizes cell movements in swarms of Myxococcus xanthus.

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| S-EPMC4246991 | biostudies-literature

Light-Triggered Carotenogenesis in Myxococcus xanthus: New Paradigms in Photosensory Signaling, Transduction and Gene Regulation.

Project description:Myxobacteria are Gram-negative δ-proteobacteria found predominantly in terrestrial habitats and often brightly colored due to the biosynthesis of carotenoids. Carotenoids are lipophilic isoprenoid pigments that protect cells from damage and death by quenching highly reactive and toxic oxidative species, like singlet oxygen, generated upon growth under light. The model myxobacterium Myxococcus xanthus turns from yellow in the dark to red upon exposure to light because of the photoinduction of carotenoid biosynthesis. How light is sensed and transduced to bring about regulated carotenogenesis in order to combat photooxidative stress has been extensively investigated in M. xanthus using genetic, biochemical and high-resolution structural methods. These studies have unearthed new paradigms in bacterial light sensing, signal transduction and gene regulation, and have led to the discovery of prototypical members of widely distributed protein families with novel functions. Major advances have been made over the last decade in elucidating the molecular mechanisms underlying the light-dependent signaling and regulation of the transcriptional response leading to carotenogenesis in M. xanthus. This review aims to provide an up-to-date overview of these findings and their significance.

| S-EPMC8156234 | biostudies-literature

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