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Myxobacteria, polarity, and multicellular morphogenesis.

ABSTRACT: Myxobacteria are renowned for the ability to sporulate within fruiting bodies whose shapes are species-specific. The capacity to build those multicellular structures arises from the ability of M. xanthus to organize high cell-density swarms, in which the cells tend to be aligned with each other while constantly in motion. The intrinsic polarity of rod-shaped cells lays the foundation, and each cell uses two polar engines for gliding on surfaces. It sprouts retractile type IV pili from the leading cell pole and secretes capsular polysaccharide through nozzles from the trailing pole. Regularly periodic reversal of the gliding direction was found to be required for swarming. Those reversals are generated by a G-protein switch which is driven by a sharply tuned oscillator. Starvation induces fruiting body development, and systematic reductions in the reversal frequency are necessary for the cells to aggregate rather than continue to swarm. Developmental gene expression is regulated by a network that is connected to the suppression of reversals.

SUBMITTER: Kaiser D

PROVIDER: S-EPMC2908774 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Myxobacteria, polarity, and multicellular morphogenesis.

Kaiser Dale D Robinson Mark M Kroos Lee L

Cold Spring Harbor perspectives in biology 20100707 8

Myxobacteria are renowned for the ability to sporulate within fruiting bodies whose shapes are species-specific. The capacity to build those multicellular structures arises from the ability of M. xanthus to organize high cell-density swarms, in which the cells tend to be aligned with each other while constantly in motion. The intrinsic polarity of rod-shaped cells lays the foundation, and each cell uses two polar engines for gliding on surfaces. It sprouts retractile type IV pili from the leadin ...[more]

PMID: 20610548

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Project description:Lost traits can reevolve, but the probability of trait reversion depends partly on a trait's genetic complexity. Myxobacterial fruiting body development is a complex trait controlled by the small RNA (sRNA) Pxr, which blocks development under conditions of nutrient abundance. In developmentally proficient strains of Myxococcus xanthus, starvation relaxes the inhibition by Pxr, thereby allowing development to proceed. In contrast, the lab-evolved strain OC does not develop because it fails to relay an early starvation signal that alleviates inhibition by Pxr. A descendant of OC, strain PX, previously reevolved developmental proficiency via a mutation in pxr that inactivates its function. A single-colony screen was used to test whether reversion of OC to developmental proficiency occurs only by mutation of pxr or might also occur through alternative regulatory loci. Five spontaneous mutants of OC that exhibited restored development were isolated, and all five showed defects in Pxr synthesis, structure, or processing, including one that incurred an eight-nucleotide deletion in pxr Two mutations occurred in the σ54 response regulator (RR) gene MXAN_1078 (named pxrR here), immediately upstream of pxr PxrR was found to positively regulate pxr transcription, presumably via the σ54 promoter of pxr Two other mutations were identified in a histidine kinase (HK) gene (MXAN_1077; named pxrK here) immediately upstream of pxrR Evolutionarily, the rate of trait restoration documented in this study suggests that reversion of social defects in natural microbial populations may be common. Molecularly, these results suggest a mechanism by which the regulatory functions of an HK-RR two-component signaling system and an sRNA are integrated to control initiation of myxobacterial development.ImportanceMany myxobacteria initiate a process of multicellular fruiting body development upon starvation, but key features of the regulatory network controlling the transition from growth to development remain obscure. Previous work with Myxococcus xanthus identified the first small RNA (sRNA) regulator (Pxr) known to serve as a gatekeeper in this life history transition, as it blocks development when nutrients are abundant. In the present study, a screen for spontaneous mutants of M. xanthus was developed that revealed a two-component system operon (encoding a histidine kinase and a σ54 response regulator) associated with the production and processing of Pxr sRNA. This discovery broadens our knowledge of early developmental gene regulation and also represents an evolutionary integration of two-component signaling and sRNA gene regulation to control a bacterial social trait.

Dataset Information

Myxobacteria, polarity, and multicellular morphogenesis.

Publications

Myxobacteria, polarity, and multicellular morphogenesis.

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