New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor

Abstract

SummaryIn 1971, Tomasz and Zanati discovered that competent pneumococci have a tendency to form aggregates when pelleted by centrifugation and resuspended in 0.01 N HCl by brief vortexing. Interestingly, no clumping was observed with parallel cultures of non-competent cells treated in the same way. We set out to elucidate the mechanism behind this striking phenomenon, and were able to show that it depends on extracellular DNA that is presumably released by socalled competence-induced cell lysis. Competenceinduced cell lysis, which was first described a few years ago, seems to rely on the concerted action of several murein hydrolases. Our results confirmed and extended previous findings by showing that competence-induced aggregation is abolished in a lytA-lytC double mutant, and absolutely requires CbpD and its N-terminal CHAP amidase domain. Furthermore, we discovered a novel competence stimulating peptide (CSP)-induced immunity protein, encoded by the early competence gene comM ( spr1762 ), which protects competent pneumococci against their own lysins. Together, the murein hydrolases and the immunity protein constitutes a CSP-controlled mechanism that allows competent pneumococci to commit fratricide by killing non-competent pneumococci sharing the same ecological niche. Through such predatory behaviour, pneumococci can get access to transforming DNA and nutrients, promote the release of virulence factors, and at the same time get rid of competitors.

Molecular Control of Bacterial Death and Lysis

“…In other words, during competence development, donor DNA is provided by heterolysis/allolysis (lysis of one bacterial cell that is caused by another cell) as opposed to autolysis (lysis of self) (101,237). Furthermore, the classic observation that competent S. pneumoniae cells tend to form aggregates when treated with mild acid (251) was found to be dependent upon the presence of a mixture of competent and noncompetent cells as well as the release of extracellular DNA (103). The phenomenon of competence-induced cell lysis was subsequently named "pneumococcal fratricide," defined as the intraspecies-specific killing of cells that occurs during the development of competence in S. pneumoniae (47,103).…”

“…Additionally, a lytA lytC double mutant displayed a near-complete abolishment of chromosomal DNA (166) and Ply (101) release. Furthermore, the LytA and LytC required during allolysis can be provided by either the competent nonlysing cells or the noncompetent cells that are targeted for killing (101,103). A third novel murein hydrolase, named choline-binding protein D (CbpD), has also been shown to be necessary for fratricide to occur during competence development (101,119).…”

Culture History and Population Heterogeneity as Determinants of Bacterial Adaptation: the Adaptomics of a Single Environmental Transition

“…Competence and DNA uptake are found in taxonomically diverse bacteria (84) and are linked to cannibalistic strategies in Streptococcus pneumoniae (128,139). Cells that are competent for natural genetic transformation lyse noncompetent cells, and virulence factors are released.…”

Deadly competition between sibling bacterial colonies

“…Although antibacterial compounds such as bacteriocins affect only similar or closely related bacteria, such ''chemical weapons'' can even be used to attack sibling cells within the same colony (37)(38)(39)). An example is ''fratricide'' in Streptococcus pneumoniae (during the transition to competence) (39)(40)(41). Another example is ''cannibalism'' in Bacillus subtilis, where bacteria during the early stages of sporulation produce chemicals that kill some siblings, which become food for the surviving bacteria (37)(38).…”