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Genetics of Natural Competence in and other Vibrios

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  • Authors: Elena S. Antonova1, Brian K. Hammer2
  • Editor: Michael Sadowsky3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720; 2: School of Biology, Georgia Institute of Technology, Atlanta, GA 30332-0230; 3: University of Minnesota, St. Paul, MN
  • Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0010-2014
  • Received 17 December 2014 Accepted 03 March 2015 Published 19 June 2015
  • Brian K. Hammer, bhammer@gatech.edu
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  • Abstract:

    Many Gram-positive and Gram-negative bacteria can become naturally competent to take up extracellular DNA from the environment via a dedicated uptake apparatus. The genetic material that is acquired can (i) be used for nutrients, (ii) aid in genome repair, and (iii) promote horizontal gene transfer when incorporated onto the genome by homologous recombination, the process of “transformation.” Recent studies have identified multiple environmental cues sufficient to induce natural transformation in and several other species. In , nutrient limitation activates the cAMP receptor protein regulator, quorum-sensing signals promote synthesis of HapR-controlled QstR, chitin stimulates production of TfoX, and low extracellular nucleosides allow CytR to serve as an additional positive regulator. The network of signaling systems that trigger expression of each of these required regulators is well described, but the mechanisms by which each in turn controls competence apparatus genes is poorly understood. Recent work has defined a minimal set of genes that encode apparatus components and begun to characterize the architecture of the machinery by fluorescence microscopy. While studies with a small set of reference isolates have identified regulatory and competence genes required for DNA uptake, future studies may identify additional genes and regulatory connections, as well as revealing how common natural competence is among diverse isolates and other species.

  • Citation: Antonova E, Hammer B. 2015. Genetics of Natural Competence in and other Vibrios. Microbiol Spectrum 3(3):VE-0010-2014. doi:10.1128/microbiolspec.VE-0010-2014.

Key Concept Ranking

Microbial Ecology
0.6351167
Furanosyl Borate Diester
0.4794825
Type IV Pili
0.43714863
Periplasmic Space
0.43043086
Scanning Electron Microscopy
0.40953615
0.6351167

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/content/journal/microbiolspec/10.1128/microbiolspec.VE-0010-2014
2015-06-19
2017-05-24

Abstract:

Many Gram-positive and Gram-negative bacteria can become naturally competent to take up extracellular DNA from the environment via a dedicated uptake apparatus. The genetic material that is acquired can (i) be used for nutrients, (ii) aid in genome repair, and (iii) promote horizontal gene transfer when incorporated onto the genome by homologous recombination, the process of “transformation.” Recent studies have identified multiple environmental cues sufficient to induce natural transformation in and several other species. In , nutrient limitation activates the cAMP receptor protein regulator, quorum-sensing signals promote synthesis of HapR-controlled QstR, chitin stimulates production of TfoX, and low extracellular nucleosides allow CytR to serve as an additional positive regulator. The network of signaling systems that trigger expression of each of these required regulators is well described, but the mechanisms by which each in turn controls competence apparatus genes is poorly understood. Recent work has defined a minimal set of genes that encode apparatus components and begun to characterize the architecture of the machinery by fluorescence microscopy. While studies with a small set of reference isolates have identified regulatory and competence genes required for DNA uptake, future studies may identify additional genes and regulatory connections, as well as revealing how common natural competence is among diverse isolates and other species.

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FIGURE 1

Schematic model of competence apparatus. Incoming dsDNA is transported across the outer membrane (OM) through the PilQ secretin aided by “pilot” protein PilP, assembly proteins PilM, PilN, PilO, and perhaps PilF (green). The pilin (shown retracted here) is composed of PilA subunits processed by the prepilin peptidase (PilD) and anchored to PilC, with assistance from the PilT and PilB (blue). Periplasmic dsDNA associates with the ComEA DNA-binding protein (orange) and has one strand degraded by nucleases. The ssDNA accesses the cytoplasm through the inner membrane (IM) ComEC channel aided by ComF (purple). Putative pilin are indicated (red). Colors correspond to genes indicated in Table 1 . doi:10.1128/microbiolspec.VE-0010-2014.f1

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0010-2014
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FIGURE 2

A model that shows multiple regulatory pathways control natural competence in . Chitin present at high levels in marine systems associates with the chitin binding protein (CBP), indirectly resulting in production of the TfoX regulator. In response to high levels of quorum-sensing autoinducers (CAI-1 and AI-2) that bind to cognate inner membrane (IM) receptor proteins, the HapR transcription factor is made. HapR directly activates transcription of the QstR regulator. CytR is present to positively control competence when extracellular levels of nucleosides are low and cytidine is not taken up by the Tsx/Nup complex. The catabolite repressor protein (CRP) plays a role in each regulatory system when glucose is scarce: associating with TfoX and CytR and enhancing levels of the CAI-1 synthase enzyme CqsA. Dashed arrows indicate where direct interactions have not been demonstrated and where additional pathway components may still be identified (see text for details). OM, outer membrane. doi:10.1128/microbiolspec.VE-0010-2014.f2

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0010-2014
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Tables

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TABLE 1

Predicted and known competence machinery and regulatory genes and orthologs in other species

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0010-2014

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