Adaptive Evolution of an sRNA That Controls
            <i>Myxococcus</i>
            Development

Yu, Yuen-Tsu N.; Yuan, Xiutang; Velicer, Gregory J.

doi:10.1126/science.1187200

Cited by 41 publications

(93 citation statements)

References 5 publications

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“…S1 in the supplemental material) echo a broader theme of plasticity in the genetic elements that underlie proficient myxobacterial development. This theme emerges from analyses that span in breadth from interspecific comparative genomic analysis (63,65) to fine-scale comparison of laboratory-evolved conspecifics that differ by only a few mutations (66,67). Several other loci important for development in M. xanthus strain DK1622 are also absent from other fruiting myxobacteria, suggesting that there are many genetically viable pathways to proficient fruiting body development (63,65).…”

Section: Figmentioning

confidence: 99%

devIIs an Evolutionarily Young Negative Regulator of Myxococcus xanthus Development

et al. 2015

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During starvation-induced development of Myxococcus xanthus, thousands of rod-shaped cells form mounds in which they differentiate into spores. The dev locus includes eight genes followed by clustered regularly interspaced short palindromic repeats (CRISPRs), comprising a CRISPR-Cas system (Cas stands for CRISPR associated) typically involved in RNA interference. Mutations in devS or devR of a lab reference strain permit mound formation but impair sporulation. We report that natural isolates of M. xanthus capable of normal development are highly polymorphic in the promoter region of the dev operon. We show that the dev promoter is predicted to be nonfunctional in most natural isolates and is dispensable for development of a laboratory reference strain. Moreover, deletion of the dev promoter or the small gene immediately downstream of it, here designated devI (development inhibitor), suppressed the sporulation defect of devS or devR mutants in the lab strain. Complementation experiments and the result of introducing a premature stop codon in devI support a model in which DevRS proteins negatively autoregulate expression of devI, whose 40-residue protein product DevI inhibits sporulation if overexpressed. DevI appears to act in a cellautonomous manner since experiments with conditioned medium and with cell mixtures gave no indication of extracellular effects. Strikingly, we report that devI is entirely absent from most M. xanthus natural isolates and was only recently integrated into the developmental programs of some lineages. These results provide important new insights into both the evolutionary history of the dev operon and its mechanistic role in M. xanthus sporulation. IMPORTANCECertain mutations in the dev CRISPR-Cas (clustered regularly interspaced short palindromic repeat-associated) system of Myxococcus xanthus impair sporulation. The link between development and a CRISPR-Cas system has been a mystery. Surprisingly, DNA sequencing of natural isolates revealed that many appear to lack a functional dev promoter, yet these strains sporulate normally. Deletion of the dev promoter or the small gene downstream of it suppressed the sporulation defect of a lab strain with mutations in dev genes encoding Cas proteins. The results support a model in which the Cas proteins DevRS prevent overexpression of the small gene devI, which codes for an inhibitor of sporulation. Phylogenetic analysis of natural isolates suggests that devI and the dev promoter were only recently acquired in some lineages. Myxococcus xanthus is a Gram-negative bacterium of the deltaproteobacteria group. Typically found in the soil, M. xanthus exhibits social behaviors (1). The rod-shaped cells move in groups on solid surfaces, feeding on prey bacteria and organic matter. When starved, cells modify their movements and build mounds containing thousands of individuals that differentiate into ovoid spores. The resulting mound of dormant and insultresistant spores is called a fruiting body. Spores within the fruiting body germinate when con...

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Section: Figmentioning

confidence: 99%

devIIs an Evolutionarily Young Negative Regulator of Myxococcus xanthus Development

et al. 2015

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“…Although our understanding of the developmental programme is far from complete, it is clear that building a multicellular fruiting body with a defined size and shape requires a regulatory network that is highly responsive to environmental, intercellular and intracellular signals (Kaiser et al, 2010). Through extensive genetic and biochemical studies, a number of factors thought to be involved in cellular aggregation and sporulation have been identified, including sigma factors, two-component proteins, s 54 -dependent enhancer-binding proteins, serine/threonine kinases, proteases, and even non-coding RNA and secondary metabolites (Kaiser et al, 2010;Meiser et al, 2006;Yu et al, 2010). In this work, we initially intended to search for regulatory genes potentially involved in controlling mcu expression; however, using transposon mutagenesis we identified MXAN3487 (MXAN_RS16905), a gene encoding a putative adenosine 59-phosphosulphate (APS) kinase (i.e.…”

Section: Introductionmentioning

confidence: 99%

A gene encoding a potential adenosine 5′-phosphosulphate kinase is necessary for timely development of Myxococcus xanthus

Wang

Song

et al. 2016

Microbiology

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A Myxococcus xanthus gene, MXAN3487, was identified by transposon mutagenesis to be required for the expression of mcuABC, an operon coding for part of the chaperone-usher (CU) system in this bacterium. The MXAN3487 protein displays sequence and structural homology to adenosine 59-phosphosulphate (APS) kinase family members and contains putative motifs for ATP and APS binding. Although the MXAN3487 locus is not linked to other sulphate assimilation genes, its protein product may have APS kinase activity in vivo and the importance of the ATP-binding site for activity was demonstrated. Expression of MXAN3487 was not affected by sulphate availability, suggesting that MXAN3487 may not function in a reductive sulphate assimilation pathway. Deletion of MXAN3487 significantly delayed fruiting body formation and the production of McuA, a spore coat protein secreted by the M. xanthus Mcu CU system. Based on these observations and data from our previous studies, we propose that MXAN3487 may phosphorylate molecules structurally related to APS, generating metabolites necessary for M. xanthus development, and that MXAN3487 exerts a positive effect on the mcuABC operon whose expression is morphogenesis dependent.

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“…If, instead, an sRNA is involved, it may be as long as the rcbA coding region (210 bp). Because point mutations in antisense RNAs have been shown to disrupt base pairing and antisense RNA functions (8,27,35,97) and may also inhibit the activity of an sRNA that interacts with a protein, we have not attempted to introduce nonsense or missense mutations into the rcbA gene. Had we introduced mutations that were inactivating, the results would not exclude the involvement of an sRNA.…”

Section: Resultsmentioning

confidence: 99%

The rcbA Gene Product Reduces Spontaneous and Induced Chromosome Breaks in Escherichia coli

Felczak

Kaguni

2012

J Bacteriol

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Elevated levels of DnaA cause excessive initiation, which leads to an increased level of double-strand breaks that are proposed to arise when newly formed replication forks collide from behind with stalled or collapsed forks. These double-strand breaks are toxic in mutants that are unable to repair them. Using a multicopy suppressor assay to identify genes that suppress this toxicity, we isolated a plasmid carrying a gene whose function had been unknown. This gene, carried by the cryptic rac prophage, has been named rcbA for its ability to reduce the frequency of chromosome breaks. Our study shows that the colony formation of strains bearing mutations in rep, recG, and rcbA, like recA and recB mutants, is inhibited by an oversupply of DnaA and that a multicopy plasmid carrying rcbA neutralizes this inhibition. These and other results suggest that rcbA helps to maintain the integrity of the bacterial chromosome by lowering the steady-state level of double-strand breaks. Chromosomal DNA replication is coordinated to occur once per cell cycle. In Escherichia coli, the initiation of DNA replication requires the recognition of specific sequences in its single replication origin (oriC) by DnaA bound to ATP, which leads to the stepwise assembly of the molecular machinery at each replication fork (reviewed in references 46, 54, and 55). One enzymatic component of this molecular machine is DnaB, the replicative helicase that unwinds the parental duplex DNA as the replication forks advance under a bidirectional mode of fork movement from oriC. Other components are a primase that forms primers on each strand of the parental template DNA for leading-and laggingstrand DNA synthesis and a dimeric DNA polymerase III holoenzyme that copies each parental DNA. Recent evidence indicates that a second DNA helicase, named Rep, interacts with DnaB to facilitate fork movement (36).Several independent mechanisms control the initiation process so that it occurs only once during each cell cycle (reviewed in references 46, 54, and 55). One mechanism involves SeqA, which specifically recognizes hemimethylated GATC sequences that transiently exist after a new round of DNA replication (59,71,73,93). The specific binding of SeqA to these sequences that are abundant in oriC is thought to sequester the replication origin from DnaA and other replication proteins (6, 71). The second mechanism requires Hda complexed with the ␤ clamp (47, 89). When bound to DNA, this complex stimulates the hydrolysis of ATP bound to DnaA. Because DnaA complexed with ATP is active in initiation, whereas DnaA-ADP is feeble, the interaction of the Hda-␤ clamp complex regulates the frequency of initiation by affecting the activity of DnaA. The third mechanism relies on a site in the bacterial chromosome named datA (48). On the basis that several hundred DnaA molecules can apparently bind at this locus and that the deletion of this site leads to extra initiations, datA was proposed to titrate DnaA when in excess to avert extra initiations. A separate mechanism also invo...

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Adaptive Evolution of an sRNA That Controls Myxococcus Development

Abstract: Mutation of a small noncoding RNA drives adaptive evolution in a social bacterium.

Cited by 41 publications

References 5 publications

devIIs an Evolutionarily Young Negative Regulator of Myxococcus xanthus Development

devIIs an Evolutionarily Young Negative Regulator of Myxococcus xanthus Development

A gene encoding a potential adenosine 5′-phosphosulphate kinase is necessary for timely development of Myxococcus xanthus

The rcbA Gene Product Reduces Spontaneous and Induced Chromosome Breaks in Escherichia coli

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