Killing niche competitors by remote-control bacteriophage induction - PubMed (original) (raw)

Killing niche competitors by remote-control bacteriophage induction

Laura Selva et al. Proc Natl Acad Sci U S A. 2009.

Abstract

A surprising example of interspecies competition is the production by certain bacteria of hydrogen peroxide at concentrations that are lethal for others. A case in point is the displacement of Staphylococcus aureus by Streptococcus pneumoniae in the nasopharynx, which is of considerable clinical significance. How it is accomplished, however, has been a great mystery, because H(2)O(2) is a very well known disinfectant whose lethality is largely due to the production of hyperoxides through the abiological Fenton reaction. In this report, we have solved the mystery by showing that H(2)O(2) at the concentrations typically produced by pneumococci kills lysogenic but not nonlysogenic staphylococci by inducing the SOS response. The SOS response, a stress response to DNA damage, not only invokes DNA repair mechanisms but also induces resident prophages, and the resulting lysis is responsible for H(2)O(2) lethality. Because the vast majority of S. aureus strains are lysogenic, the production of H(2)O(2) is a very widely effective antistaphylococcal strategy. Pneumococci, however, which are also commonly lysogenic and undergo SOS induction in response to DNA-damaging agents such as mitomycin C, are not SOS-induced on exposure to H(2)O(2). This is apparently because they are resistant to the DNA-damaging effects of the Fenton reaction. The production of an SOS-inducing signal to activate prophages in neighboring organisms is thus a rather unique competitive strategy, which we suggest may be in widespread use for bacterial interference. However, this strategy has as a by-product the release of active phage, which can potentially spread mobile genetic elements carrying virulence genes.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Killing of S. aureus by H2O2. Survival of lysogenic (COL, Mu50, FRI-S6, RF122, LUG855, and RN10359) or nonlysogenic (V329, RN450) S. aureus strains in media supplemented with hydrogen peroxide at a concentration of 0.5 mM, and unsupplemented medium (control). Values represent the average of 3 independent experiments. Variation was within ± 5% in all cases.

Fig. 2.

Fig. 2.

Lysis of S. pneumoniae induced by mitomycin C or H2O2. Cultures of lysogenic (623 and 949) or nonlysogenic (TIGR4) strains received mitomycin C (0.1 μg/mL) or H2O2 (0.5 mM) at time 0, and the OD of cultures was monitored at 600 nm.

Fig. 3.

Fig. 3.

Role of catalase in SOS induction by H2O2. (A) Survival of S. aureus strains in media supplemented with hydrogen peroxide at different concentrations. Values represent the average of 3 independent experiments. Variation was within ±5% in all cases. (B) Phage titer obtained from the lysogenic strains analyzed in A.

Fig. 4.

Fig. 4.

Killing of lysogenic S. aureus cells by antibiotics. (A) Survival S. aureus strains in media supplemented with different concentrations of the antibiotic ciprofloxacin. RN450, nonlysogenic; RN10359, RN450 lysogenic for phage 80α; RN10359 cI−, derivative of RN10359 carrying a non-SOS-inducible phage 80α; RN451, RN450 lysogenic for phage 11; RN451 cI−, derivative of RN451 carrying a non-SOS-inducible phage 11. Values represent the average of 3 independent experiments. Variation was within ± 5% in all cases. (B) Antibiogram showing the different susceptibility between strains RN10359 (lysogenic for phage 80α) and RN10359 cI− (carrying a non-SOS-inducible phage 80α) to enrofloxacin discs. Average zone of inhibition: RN10359, 36 mm; RN10359 cI−, 30 mm.

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