Synthesis and Assembly of a Novel Glycan Layer in Myxococcus xanthus Spores

Holkenbrink, Carina; Hoiczyk, Egbert; Kahnt, Jörg; Higgs, Penelope I.

doi:10.1074/jbc.m114.595504

Cited by 36 publications

(103 citation statements)

References 62 publications

(51 reference statements)

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“…Expression of the nfs promoter fused to an mCherry reporter gene was reduced in a devRS mutant (36). Nfs proteins appear to work together with Exo proteins to form the polysaccharide spore coat (27,37,38). Positive regulation of exo, nfs, and perhaps other genes by DevTRS suggests a general mechanism of control.…”

Section: Discussionmentioning

confidence: 92%

The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development

Rajagopalan

Kroos

2017

J Bacteriol

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Myxococcus xanthus undergoes multicellular development when starved. Thousands of rod-shaped cells coordinate their movements and aggregate into mounds in which cells differentiate into spores. Mutations in the dev operon impair development. The dev operon encompasses a clustered regularly interspaced short palindromic repeat-associated (CRISPR-Cas) system. Null mutations in devI, a small gene at the beginning of the dev operon, suppress the developmental defects caused by null mutations in the downstream devR and devS genes but failed to suppress defects caused by a small in-frame deletion in devT. We provide evidence that the original mutant has a second-site mutation. We show that devT null mutants exhibit developmental defects indistinguishable from devR and devS null mutants, and a null mutation in devI suppresses the defects of a devT null mutation. The similarity of DevTRS proteins to components of the CRISPR-associated complex for antiviral defense (Cascade), together with our molecular characterization of dev mutants, support a model in which DevTRS form a Cascade-like subcomplex that negatively autoregulates dev transcript accumulation and prevents DevI overproduction that would strongly inhibit sporulation. Our results also suggest that DevI transiently inhibits sporulation when regulated normally. The mechanism of transient inhibition may involve MrpC, a key transcription factor, whose translation appears to be weakly inhibited by DevI. Finally, our characterization of a devI devS mutant indicates that very little exo transcript is required for sporulation, which is surprising since Exo proteins help form the polysaccharide spore coat.IMPORTANCE CRISPR-Cas systems typically function as adaptive immune systems in bacteria. The dev CRISPR-Cas system of M. xanthus has been proposed to prevent bacteriophage infection during development, but how dev controls sporulation has been elusive. Recent evidence supported a model in which DevR and DevS prevent overproduction of DevI, a predicted 40-residue inhibitor of sporulation. We provide genetic evidence that DevT functions together with DevR and DevS to prevent DevI overproduction. We also show that spores form about 6 h earlier in mutants lacking devI than in the wild type. Only a minority of natural isolates appear to have a functional dev promoter and devI, suggesting that a functional dev CRISPR-Cas system evolved recently in niches where delayed sporulation and/or protection from bacteriophage infection proved advantageous.KEYWORDS CRISPR-Cas, Myxococcus xanthus, bacterial development, dev operon, gene regulation, signaling, sporulation M yxococcus xanthus is a Gram-negative soil bacterium that exhibits social behaviors (1). In nature, cells of M. xanthus move in groups, feeding on prey bacteria and organic detritus. When starved, thousands of cells aggregate to form mounds that mature into fruiting bodies as rod-shaped cells differentiate into dormant ovoid spores.

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Section: Discussionmentioning

confidence: 92%

The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development

Rajagopalan

Kroos

2017

J Bacteriol

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“…Specifically, the Agl machinery is responsible for rotating the Nfs protein complex around the cell envelope during sporulation (Wartel et al, 2013). Shape change is followed by production of a thick outer wall consisting of the spore coat protein S, in addition to glycosaminoglycan, N-acetylgalactosamine, glucose and glycine (Inouye et al, 1981;Kottel et al, 1975;Holkenbrink et al, 2014). Together, these changes allow spores to survive harsh environmental conditions in a dormant state.…”

Section: Fruiting Behaviourmentioning

confidence: 99%

The predatory life cycle of Myxococcus xanthus

Keane

Berleman

2016

Microbiology

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“…Cells move in travelling waves or ripples (Shimkets and Kaiser 1982), form evenly spaced multicellular aggregates known as fruiting bodies (Xie et al 2011), and differentiate into dormant spores within these aggregates (Holkenbrink et al 2014). Several differentiating cell types are produced, leading to programmed cell death (PCD), sporulation, and production of peripheral rods (O'Connor and Zusman 1991;Boynton et al 2013).…”

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confidence: 99%

Myxococcus CsgA, Drosophila Sniffer, and human HSD10 are cardiolipin phospholipases

Boynton

Shimkets

2015

Genes Dev.

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Myxococcus xanthus development requires CsgA, a member of the short-chain alcohol dehydrogenase (SCAD) family of proteins. We show that CsgA and SocA, a protein that can replace CsgA function in vivo, oxidize the 2 ′ -OH glycerol moiety on cardiolipin and phosphatidylglycerol to produce diacylglycerol (DAG), dihydroxyacetone, and orthophosphate. A lipid extract enriched in DAGs from wild-type cells initiates development and lipid body production in a csgA mutant to bypass the mutational block. This novel phospholipase C-like reaction is widespread. SCADs that prevent neurodegenerative disorders, such as Drosophila Sniffer and human HSD10, oxidize cardiolipin with similar kinetic parameters. HSD10 exhibits a strong preference for cardiolipin with oxidized fatty acids. This activity is inhibited in the presence of the amyloid β peptide. Three HSD10 variants associated with neurodegenerative disorders are inactive with cardiolipin. We suggest that HSD10 protects humans from reactive oxygen species by removing damaged cardiolipin before it induces apoptosis.

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Synthesis and Assembly of a Novel Glycan Layer in Myxococcus xanthus Spores

Cited by 36 publications

References 62 publications

The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development

The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development

The predatory life cycle of Myxococcus xanthus

Myxococcus CsgA, Drosophila Sniffer, and human HSD10 are cardiolipin phospholipases

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