More than Simple Parasites: the Sociobiology of Bacteriophages and Their Bacterial Hosts

Abstract

Bacteria harbor viruses called bacteriophages that, like all viruses, co-opt the host cellular machinery to replicate. Although this relationship is at first glance parasitic, there are social interactions among and between bacteriophages and their bacterial hosts. These social interactions can take on many forms, including cooperation, altruism, and cheating. Such behaviors among individuals in groups of bacteria have been well described. However, the social nature of some interactions between phages or phages and bacteria is only now becoming clear. We are just beginning to understand how bacteriophages affect the sociobiology of bacteria, and we know even less about social interactions within bacteriophage populations. In this review, we discuss recent developments in our understanding of bacteriophage sociobiology, including how selective pressures influence the outcomes of social interactions between populations of bacteria and bacteriophages. We also explore how tripartite social interactions between bacteria, bacteriophages, and an animal host affect host-microbe interactions. Finally, we argue that understanding the sociobiology of bacteriophages will have implications for the therapeutic use of bacteriophages to treat bacterial infections.

Keywords: bacteria; bacteriophage; cheater; cooperation; sociobiology.

FIG 1

Pools of public goods provide incentive for bacteriophages to cheat. As bacteriophages replicate inside an infected cell, pools of public goods such as enzymes and capsid proteins are produced. Bacteriophages, like all viruses, have a high mutational rate, and cheaters can emerge that either do not contribute to public-good production or consume public goods (i.e., assemble complete virions) at a higher rate than ancestral bacteriophages. When the incentive to cheat is sufficiently high, cheater populations (shown in red) can expand.

FIG 2

Pf4 miniphage cheaters emerge in serially passaged cultures. (A) Model depicting how Pf miniphages could emerge and propagate. (B) Episomal Pf DNA was isolated from P. aeruginosa cultures infected by serially passaged Pf. A dominant and stable subpopulation of miniphages with a 2.5-kbp genome was established after the second passage. (C) The dominant Pf miniphage genome is predicted to be composed of only intergenic features required for DNA replication and packaging into phage particles, similar to features of M13 miniphages. All other phage components such as capsid proteins are provided by low copy numbers of full-length phage coinfecting the same cell.

FIG 3

Bacteriophages can suppress, expand, or stabilize bacterial cheater populations. Strong social selection here refers to a selective pressure (such as iron limitation) that promotes the expansion of bacterial cheater populations. (A) When selection for bacteriophage-resistant individuals is stronger than selection for cheaters (red cells), bacteriophage resistance mutations (stripped cells) propagate at a higher rate through the numerically dominant cooperator population (blue cells) than in the emerging cheater population. (B) When the incentive to cheat outweighs the selective pressures of bacteriophage predation, cheater populations can expand to the point of population collapse. (C) Transposable bacteriophages randomly integrate into the bacterial chromosome and drive bacterial diversification. Coupled with a strong social selective pressure, infection by a transposable bacteriophage can promote a divergent social strategy wherein both cheaters and public-good overproducers emerge to stabilize the bacterial population.