The population biology of bacterial viruses: Why be temperate

Abstract

A model of the interactions between populations of temperate and virulent bacteriophage with sensitive, lysogenic, and resistant bacteria is presented. In the analysis of the properties of this model, particular consideration is given to the conditions under which temperate bacteriophage can become established and will be maintained in bacterial populations. The effects of the presence of resistant bacteria and virulent phage on these “existence” conditions for temperate viruses are considered. It is demonstrated that under broad conditions temperate phage will be maintained in bacterial populations and will coexist with virulent phage. Extrapolating from this formal consideration of the population biology of temperate bacteriophage, a number of hypotheses for the conditions under which temperate, rather than virulent, modes of phage reproduction are to be anticipated and the nature of the selective pressures leading to the evolution and persistence of this “benign” type of bacterial virus are reviewed and critically evaluated. Two hypotheses for the “advantages of temperance” are championed: (1) As a consequence of the allelopathic effects of diffusing phage, in physically structured habitats, lysogenic colonies are able to sequester resources and, in that way, have an advantage when competing with sensitive nonlysogens. (2) Lysogeny is an adaptation for phage to maintain their populations in “hard times,” when the host bacterial density oscillates below that necessary for phage to be maintained by lytic infection alone.