Diverse Bacteriophage Roles in an Aphid-Bacterial Defensive Mutualism

Abstract

Despite the well-described importance of bacteriophages to bacterial pathogens, little is known about their influence on the many bacterial species that form beneficial symbioses with eukaryotes. Most insect species, for example, are infected with one or more maternally inherited symbionts, which provide nutritional and defensive services in exchange for housing. The pea aphid, Acyrthosiphon pisum, harbors at least seven common heritable symbionts that mediate a range of ecological interactions and has emerged as a model for studies of beneficial symbionts. One common pea aphid defensive symbiont, Hamiltonella defensa, protects against parasitic wasps, which are important natural enemies. The bacterium is itself infected by temperate bacteriophages, called APSEs (Acyrthosiphon pisum secondary endosymbionts), which are necessary for H. defensa-mediated protection. This represents the first known instance of a bacteria-insect mutualism requiring a viral partner. APSEs play other key roles in the regulation and maintenance of H. defensa: APSE loss results in high titers of the bacterial symbiont, which is correlated with severe fitness costs to the aphid host. These costs to the aphid incurred by phage loss likely lead to phage-free H. defensa- infected aphids being rapidly removed from the population, thus limiting the invasion potential of H. defensa. Below we review the roles of APSEs in the H. defensa-aphid defensive symbiosis and suggest a framework for future studies. We then make comparisons with another well-studied phage-symbiont interaction (Wolbachia-WO) and consider the roles of bacteriophages in the evolution of heritable symbioses and how they may influence other insect-associated bacteria, such as the gut microbiota.