<scp><i>R</i></scp><i>hodobacter capsulatus</i> <scp>DprA</scp> is essential for <scp>RecA</scp>‐mediated gene transfer agent (<scp>RcGTA</scp>) recipient capability regulated by quorum‐sensing and the <scp>CtrA</scp> response regulator

Brimacombe, Cedric A.; Ding, Hao; Beatty, J. Thomas

doi:10.1111/mmi.12628

Cited by 49 publications

(53 citation statements)

References 75 publications

(190 reference statements)

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“…DprA, which preferentially binds ssDNA (7,37,40) and physically interacts with SsbB and RecA in vivo (5) and with RecA in vitro (7,8,41,42), has two activities: to mediate annealing of two complementary strands coated by SsbB and to a lesser extent by SsbA or naked ssDNA and to recruit RecA⅐dATP onto SsbB-or SsbA-coated ssDNA (7). The first activity is required for the annealing of the incoming oligomeric plasmid ssDNA to reconstitute a dsDNA circular plasmid molecule (plasmid transformation) (7).…”

Section: Discussionmentioning

confidence: 99%

Roles of Bacillus subtilis DprA and SsbA in RecA-mediated Genetic Recombination

Yadav

Carrasco

Serrano

et al. 2014

Journal of Biological Chemistry

102

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Section: Discussionmentioning

confidence: 99%

Roles of Bacillus subtilis DprA and SsbA in RecA-mediated Genetic Recombination

Yadav

Carrasco

Serrano

et al. 2014

Journal of Biological Chemistry

102

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“…Genetic analysis showed that one of these genes, dprA, is essential for RcGTA recipient capability, as is the RecA homologue (13). These findings indicated that RcGTA-carried DNA recombines into the chromosome of recipient cells via a natural transformation-like mechanism rather than one resembling temperate phages (20,21).…”

mentioning

confidence: 75%

“…Instead, ComM homologues are detectable only in genomes in which the corresponding DprA homologue contains a DprA domain 3 (DD3) (see Fig. S1), which is predicted to confer dsDNA binding capability to DprA proteins (13). Based on these analyses, we speculate that ComM is involved in a recombination step within the cytoplasm of recipient cells, and that its function is related to the DD3 (13,18).…”

Section: Resultsmentioning

confidence: 99%

“…These findings indicated that RcGTA-carried DNA recombines into the chromosome of recipient cells via a natural transformation-like mechanism rather than one resembling temperate phages (20,21). However, it was unknown whether three other homologues of natural competence genes downregulated in a ctrA mutant, namely, comEC, comF, and comM, were involved in RcGTA recipient capability (13).…”

mentioning

confidence: 98%

“…Production of RcGTA requires the CtrA response regulator, and transcription is modulated by the GtaI/R quorumsensing system (10)(11)(12). The ability of cells to receive an RcGTA-carried genetic marker also is regulated by CtrA and quorum sensing, and in recipient cells DNA recombination occurs via a RecA/ DprA recombination mechanism as in natural transformation systems (13).…”

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confidence: 99%

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Homologues of Genetic Transformation DNA Import Genes Are Required for Rhodobacter capsulatus Gene Transfer Agent Recipient Capability Regulated by the Response Regulator CtrA

et al. 2015

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Gene transfer agents (GTAs) morphologically resemble small, double-stranded DNA (dsDNA) bacteriophages; however, their only known role is to package and transfer random pieces of the producing cell genome to recipient cells. The best understood GTA is that of Rhodobacter capsulatus, termed RcGTA. We discovered that homologues of three genes involved in natural transformation in other bacteria, comEC, comF, and comM, are essential for RcGTA-mediated gene acquisition. This paper gives genetic and biochemical evidence that RcGTA-borne DNA entry into cells requires the ComEC and ComF putative DNA transport proteins and genetic evidence that putative cytoplasmic ComM protein of unknown function is required for recipient capability. Furthermore, the master regulator of RcGTA production in <1% of a cell population, CtrA, which is also required for gene acquisition in recipient cells, is expressed in the vast majority of the population. Our results indicate that RcGTA-mediated gene transfer combines key aspects of two bacterial horizontal gene transfer mechanisms, where donor DNA is packaged in transducing phage-like particles and recipient cells take up DNA using natural transformation-related machinery. Both of these differentiated subsets of a culture population, donors and recipients, are dependent on the same response regulator, CtrA. IMPORTANCEHorizontal gene transfer (HGT) is a major driver of bacterial evolution and adaptation to environmental stresses. Traits such as antibiotic resistance or metabolic properties can be transferred between bacteria via HGT; thus, HGT can have a tremendous effect on the fitness of a bacterial population. The three classically described HGT mechanisms are conjugation, transformation, and phage-mediated transduction. More recently, the HGT factor GTA was described, where random pieces of producing cell genome are packaged into phage-like particles that deliver DNA to recipient cells. In this report, we show that transport of DNA borne by the R. capsulatus RcGTA into recipient cells requires key genes previously thought to be specific to natural transformation pathways. These findings indicate that RcGTA combines central aspects of phage-mediated transduction and natural transformation in an efficient, regulated mode of HGT.T he first evidence of prokaryotic genetic exchange was transformation, a term coined in 1928 by Griffith (1). Subsequently, conjugation was observed in 1946 (2), followed by transduction, which was discovered in 1952 (3). More recently, another prokaryotic mode of horizontal gene transfer, dependent on an extracellular particle called a gene transfer agent (GTA), was described (4), and GTAs subsequently have been discovered in diverse prokaryotes (5).GTAs varying in morphology have been reported, although most resemble small, tailed double-stranded DNA (dsDNA) bacteriophages. The general criteria that define a GTA are (i) the DNA packaged within the head is insufficient to carry the GTA structural genes; (ii) all GTA particles package only random parts o...

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“You produce while I clean up”, a strategy revealed by exoproteomics during Synechococcus–Roseobacter interactions

2015

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Most of the energy that is introduced into the oceans by photosynthetic primary producers is in the form of organic matter that then sustains the rest of the food web, from micro to macro‐organisms. However, it is the interactions between phototrophs and heterotrophs that are vital to maintaining the nutrient balance of marine microbiomes that ultimately feed these higher trophic levels. The primary produced organic matter is mostly remineralized by heterotrophic microorganisms but, because most of the oceanic dissolved organic matter is in the form of biopolymers, and microbial membrane transport systems operate with molecules <0.6 kDa, it must be hydrolyzed outside the cell before a microorganism can acquire it. As a simili of the marine microbiome, we analyzed, using state‐of‐the‐art proteomics, the exoproteomes obtained from synthetic communities combining specific Roseobacter (Ruegeria pomeroyi DSS‐3, Roseobacter denitrificans OCh114, and Dinoroseobacter shibae DFL‐12) and Synechococcus strains (WH7803 and WH8102). This approach identified the repertoire of hydrolytic enzymes secreted by Roseobacter, opening up the black box of heterotrophic transformation/remineralization of biopolymers generated by marine phytoplankton. As well as highlighting interesting exoenzymes this strategy also allowed us to infer clues on the molecular basis of niche partitioning.

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Rhodobacter capsulatus DprA is essential for RecA‐mediated gene transfer agent (RcGTA) recipient capability regulated by quorum‐sensing and the CtrA response regulator

Cited by 49 publications

References 75 publications

Roles of Bacillus subtilis DprA and SsbA in RecA-mediated Genetic Recombination

Roles of Bacillus subtilis DprA and SsbA in RecA-mediated Genetic Recombination

Homologues of Genetic Transformation DNA Import Genes Are Required for Rhodobacter capsulatus Gene Transfer Agent Recipient Capability Regulated by the Response Regulator CtrA

“You produce while I clean up”, a strategy revealed by exoproteomics during Synechococcus–Roseobacter interactions

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