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Global analysis of phase variation in Myxococcus xanthus.

ABSTRACT: Myxococcus xanthus can vary its phenotype or 'phase' to produce colonies that contain predominantly yellow or tan cells that differ greatly in their abilities to swarm, survive and develop. Yellow variants are proficient at swarming (++) and tend to lyse in liquid during stationary phase. In contrast, tan variants are deficient in swarming (+) and persist beyond stationary phase. The phenotypes and transcriptomes of yellow and tan variants were compared with mutants affected in phase variation. Thirty-seven genes were upregulated specifically in yellow variants including those for production of the yellow pigment, DKxanthene. A mutant in DKxanthene synthesis produced non-pigmented (tan) colonies but still phase varied for swarming suggesting that pigmentation is not the cause of phase variation. Disruption of a gene encoding a HTH-Xre-like regulator, highly expressed in yellow variants, abolished pigment production and blocked the ability of cells to switch from a swarm ++ to a swarm (+) phenotype, showing that HTH-Xre regulates phase variation. Among the four genes whose expression was increased in tan variants was pkn14, which encodes a serine-threonine kinase that regulates programmed cell death in Myxococcus via the MrpC-MazF toxin-antitoxin complex. High levels of phosphorylated Pkn14 may explain why tan cells enjoy enhanced survival.

SUBMITTER: Furusawa G

PROVIDER: S-EPMC3192537 | biostudies-literature | 2011 Aug

REPOSITORIES: biostudies-literature

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Global analysis of phase variation in Myxococcus xanthus.

Furusawa Gou G Dziewanowska Katarzyna K Stone Hannah H Settles Matthew M Hartzell Patricia P

Molecular microbiology 20110704 3

Myxococcus xanthus can vary its phenotype or 'phase' to produce colonies that contain predominantly yellow or tan cells that differ greatly in their abilities to swarm, survive and develop. Yellow variants are proficient at swarming (++) and tend to lyse in liquid during stationary phase. In contrast, tan variants are deficient in swarming (+) and persist beyond stationary phase. The phenotypes and transcriptomes of yellow and tan variants were compared with mutants affected in phase variation. ...[more]

PMID: 21722202

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Project description:BackgroundThe Myxococcales are well known for their predatory and developmental social processes, and for the molecular complexity of regulation of these processes. Many species within this order have unusually large genomes compared to other bacteria, and their genomes have many genes that are unique to one specific sequenced species or strain. Here, we describe RNAseq based transcriptome analysis of the FruA regulon of Myxococcus xanthus and a comparative RNAseq analysis of two Myxococcus species, M. xanthus and Myxococcus stipitatus, as they respond to starvation and begin forming fruiting bodies.ResultsWe show that both species have large numbers of genes that are developmentally regulated, with over half the genome showing statistically significant changes in expression during development in each species. We also included a non-fruiting mutant of M. xanthus that is missing the transcriptional regulator FruA to identify the direct and indirect FruA regulon and to identify transcriptional changes that are specific to fruiting and not just the starvation response. We then identified Interpro gene ontologies and COG annotations that are significantly up- or down-regulated during development in each species. Our analyses support previous data for M. xanthus showing developmental upregulation of signal transduction genes, and downregulation of genes related to cell-cycle, translation, metabolism, and in some cases, DNA replication. Gene expression in M. stipitatus follows similar trends. Although not all specific genes show similar regulation patterns in both species, many critical developmental genes in M. xanthus have conserved expression patterns in M. stipitatus, and some groups of otherwise unstudied orthologous genes share expression patterns.ConclusionsBy identifying the FruA regulon and identifying genes that are similarly and uniquely regulated in two different species, this work provides a more complete picture of transcription during Myxococcus development. We also provide an R script to allow other scientists to mine our data for genes whose expression patterns match a user-selected gene of interest.

Project description:BACKGROUND: Myxococcus xanthus is a Gram negative bacterium that can differentiate into metabolically quiescent, environmentally resistant spores. Little is known about the mechanisms involved in differentiation in part because sporulation is normally initiated at the culmination of a complex starvation-induced developmental program and only inside multicellular fruiting bodies. To obtain a broad overview of the sporulation process and to identify novel genes necessary for differentiation, we instead performed global transcriptome analysis of an artificial chemically-induced sporulation process in which addition of glycerol to vegetatively growing liquid cultures of M. xanthus leads to rapid and synchronized differentiation of nearly all cells into myxospore-like entities. RESULTS: Our analyses identified 1 486 genes whose expression was significantly regulated at least two-fold within four hours of chemical-induced differentiation. Most of the previously identified sporulation marker genes were significantly upregulated. In contrast, most genes that are required to build starvation-induced multicellular fruiting bodies, but which are not required for sporulation per se, were not significantly regulated in our analysis. Analysis of functional gene categories significantly over-represented in the regulated genes, suggested large rearrangements in core metabolic pathways, and in genes involved in protein synthesis and fate. We used the microarray data to identify a novel operon of eight genes that, when mutated, rendered cells unable to produce viable chemical- or starvation-induced spores. Importantly, these mutants displayed no defects in building fruiting bodies, suggesting these genes are necessary for the core sporulation process. Furthermore, during the starvation-induced developmental program, these genes were expressed in fruiting bodies but not in peripheral rods, a subpopulation of developing cells which do not sporulate. CONCLUSIONS: These results suggest that microarray analysis of chemical-induced spore formation is an excellent system to specifically identify genes necessary for the core sporulation process of a Gram negative model organism for differentiation.

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Global analysis of phase variation in Myxococcus xanthus.

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Global analysis of phase variation in Myxococcus xanthus.

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