Temperate bacterial viruses as double-edged swords in bacterial warfare

PLoS One. 2013;8(3):e59043. doi: 10.1371/journal.pone.0059043. Epub 2013 Mar 11.

Abstract

It has been argued that bacterial cells may use their temperate viruses as biological weapons. For instance, a few bacterial cells among a population of lysogenic cells could release the virus and kill susceptible non-lysogenic competitors, while their clone mates would be immune. Because viruses replicate inside their victims upon infection, this process would amplify their number in the arena. Sometimes, however, temperate viruses spare recipient cells from death by establishing themselves in a dormant state inside cells. This phenomenon is called lysogenization and, for some viruses such as the λ virus, the probability of lysogenization increases with the multiplicity of infection. Therefore, the amplification of viruses leads to conflicting predictions about the efficacy of temperate viruses as biological weapons: amplification can increase the relative advantage of clone mates of lysogens but also the likelihood of saving susceptible cells from death, because the probability of lysogenization is higher. To test the usefulness of viruses as biological weapons, we performed competition experiments between lysogenic Escherichia coli cells carrying the λ virus and susceptible λ-free E. coli cells, either in a structured or unstructured habitat. In structured and sometimes in unstructured habitats, the λ virus qualitatively behaved as a "replicating toxin". However, such toxic effect of λ viruses ceased after a few days of competition. This was due to the fact that many of initially susceptible cells became lysogenic. Massive lysogenization of susceptible cells occurred precisely under the conditions where the amplification of the virus was substantial. From then on, these cells and their descendants became immune to the λ virus. In conclusion, if at short term bacterial cells may use temperate viruses as biological weapons, after a few days only the classical view of temperate bacterial viruses as parasitic agents prevails.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteriolysis
  • Bacteriophage lambda / physiology
  • Bacteriophages / physiology*
  • Biological Warfare*
  • Drug Resistance, Bacterial
  • Escherichia coli / drug effects
  • Escherichia coli / genetics
  • Escherichia coli / virology
  • Lysogeny*
  • Streptomycin / pharmacology

Substances

  • Streptomycin

Grant support

This work was supported by Fundação para a Ciência e Tecnologia (http://alfa.fct.mctes.pt/): a Ph.D. fellowship to ILD (SFRH/BD/82375/2011)and projects EXPL/BIA-EVF/1281/2012, PTDC/BIA-BDE/66180/2006 and TECH/2007/0001, as well to the TECT-European Science Foundation program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.