Coordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighboring species. Mol Microbiol

Department of Oral Biology and Medicine, UCLA School of Dentistry, P.O. Box 951668, Los Angeles, CA 90095-1668, USA.
Molecular Microbiology (Impact Factor: 4.42). 08/2005; 57(2):392-404. DOI: 10.1111/j.1365-2958.2005.04695.x
Source: PubMed


It is important to ensure DNA availability when bacterial cells develop competence. Previous studies in Streptococcus pneumoniae demonstrated that the competence-stimulating peptide (CSP) induced autolysin production and cell lysis of its own non-competent cells, suggesting a possible active mechanism to secure a homologous DNA pool for uptake and recombination. In this study, we found that in Streptococcus mutans CSP induced co-ordinated expression of competence and mutacin production genes. This mutacin (mutacin IV) is a non-lantibiotic bacteriocin which kills closely related Streptococcal species such as S. gordonii. In mixed cultures of S. mutans and S. gordonii harbouring a shuttle plasmid, plasmid DNA transfer from S. gordonii to S. mutans was observed in a CSP and mutacin IV-dependent manner. Further analysis demonstrated an increased DNA release from S. gordonii upon addition of the partially purified mutacin IV extract. On the basis of these findings, we propose that Streptococcus mutans, which resides in a multispecies oral biofilm, may utilize the competence-induced bacteriocin production to acquire transforming DNA from other species living in the same ecological niche. This hypothesis is also consistent with a well-known phenomenon that a large genomic diversity exists among different S. mutans strains. This diversity may have resulted from extensive horizontal gene transfer.

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Available from: Jens Kreth, Oct 09, 2015
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    • "In contrast to ComRS inactivation, deletion of blpCHR do not completely abolish competence development in S. mutans in those growth conditions, and the impact on transformability is also largely strain-dependent (Ahn et al., 2006; Mashburn-Warren et al., 2010). The current mechanism of competence activation by blpCHR is the following (Fig. 5): in response to cell density (Aspiras et al., 2004; Li et al., 2001, 2002; Merritt et al., 2007) or some stress signals (Perry et al., 2009b), BIP indirectly coordinates mutacin production and comX expression (Kreth et al., 2005; van der Ploeg, 2005) in a mechanism that neither involves extracellular XIP, nor the Opp/Ami transporter (Son et al., 2012), but still requires functional comRS genes (Khan et al., 2012; Mashburn-Warren et al., 2010; Son et al., 2012; Wenderska et al., 2012). Deletion of the pre-mutacin V gene cipB (nlmC) or over-expression of the corresponding self-immunity peptide CipI, two direct targets of BlpCHR regulation, severely impairs BIP-dependent competence induction (Dufour et al., 2011). "
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    ABSTRACT: Natural DNA transformation is a lateral gene transfer mechanism during which bacteria take up naked DNA from their environment and stably integrate it in their genome. The proteins required for this process are conserved between species and are produced during a specific physiological state known as competence. Although natural transformation drives genome plasticity and adaptability, it is also likely to cause deleterious effects in the chromosome of the recipient bacteria and negatively impact cell growth. The competence window is thus generally tightly regulated in response to species-specific environmental conditions and limited to a proportion of the cell population. In streptococci species, the entry into competence is dictated by the amount of the competence sigma factor σ(X), the master regulator of natural transformation in those species. The Streptococcus genus includes 7 phylogenetic groups that have evolved different regulatory circuits to govern natural transformation. Here, we review the current knowledge on transcriptional and post-transcriptional mechanisms that control the activity of σ(X) at the whole population and the single-cell level, with an emphasis on growth conditions that modulate their activation. Recent findings regarding competence regulation by the ComCDE and ComRS cell-cell signalling pathways and the Clp proteolytic system are specifically highlighted.
    Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases 09/2014; 33. DOI:10.1016/j.meegid.2014.09.010 · 3.02 Impact Factor
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    • "That bacterial competition causes the release of DNA has been shown (Kreth et al., 2005a; Johnsborg et al., 2008). Initial investigations between the clinically relevant antagonism of S. mutans and oral commensal S. gordonii have revealed an interesting mechanism of eDNA release. "
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    ABSTRACT: The oral microbiome is composed of a multitude of different species of bacteria, each capable of occupying one or more of the many different niches found within the human oral cavity. This community exhibits many types of complex interactions which enable it to colonize and rapidly respond to changes in the environment in which they live. One of these interactions is the transfer, or acquisition, of DNA within this environment, either from co-resident bacterial species or from exogenous sources. Horizontal gene transfer in the oral cavity gives some of the resident bacteria the opportunity to sample a truly enormous metagenome affording them considerable adaptive potential which may be key to survival in such a varying environment. In this review the underlying mechanisms of HGT are discussed in relation to the oral microbiome with numerous examples described where the direct acquisition of exogenous DNA has contributed to the fitness of the bacterial host within the human oral cavity.
    Frontiers in Cellular and Infection Microbiology 09/2014; 4:124. DOI:10.3389/fcimb.2014.00124 · 3.72 Impact Factor
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    • "It is well known that oral streptococci are naturally competent, and it is possible that the DNA in the extracellular matrix is transmitted among them (Warburton et al., 2007). A study reported by Kreth et al. (2005b) proposed that S. mutans might utilize competence-induced bacteriocin to kill and lyse the neighboring species colonizing the same ecological niche and take up their DNA. Besides streptococci, P. gingivalis is able to exchange fimbrial allele types I and IV via natural competence as an adaptive process to modify behavior (Kerr et al., 2014). "
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    ABSTRACT: The oral cavity contains more than 700 microbial species that are engaged in extensive cell-cell interactions. These interactions contribute to the formation of highly structured multispecies communities, allow them to perform physiological functions, and induce synergistic pathogenesis. Co-adhesion between oral microbial species influences their colonization of oral cavity and effectuates, to a large extent, the temporal and spatial formation of highly organized polymicrobial community architecture. Individual species also compete and collaborate with other neighboring species through metabolic interactions, which not only modify the local microenvironment such as pH and the amount of oxygen, making it more suitable for the growth of other species, but also provide a metabolic framework for the participating microorganisms by maximizing their potential to extract energy from limited substrates. Direct physical contact of bacterial species with its neighboring co-habitants within microbial community could initiate signaling cascade and achieve modulation of gene expression in accordance with different species it is in contact with. In addition to communication through cell-cell contact, quorum sensing (QS) mediated by small signaling molecules such as competence-stimulating peptides (CSPs) and autoinducer-2 (AI-2), plays essential roles in bacterial physiology and ecology. This review will summarize the evidence that oral microbes participate in intercellular communications with co-inhabitants through cell contact-dependent physical interactions, metabolic interdependencies, as well as coordinative signaling systems to establish and maintain balanced microbial communities.
    Frontiers in Microbiology 07/2014; 5:328. DOI:10.3389/fmicb.2014.00328 · 3.99 Impact Factor
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