Bacteriophages encode factors required for protection in a symbiotic mutualism

Abstract

Bacteriophages are known to carry key virulence factors for pathogenic bacteria, but their roles in symbiotic bacteria are less well understood. The heritable symbiont Hamiltonella defensa protects the aphid Acyrthosiphon pisum from attack by the parasitoid Aphidius ervi by killing developing wasp larvae. In a controlled genetic background, we show that a toxin-encoding bacteriophage is required to produce the protective phenotype. Phage loss occurs repeatedly in laboratory-held H. defensa-infected aphid clonal lines, resulting in increased susceptibility to parasitism in each instance. Our results show that these mobile genetic elements can endow a bacterial symbiont with benefits that extend to the animal host. Thus, phages vector ecologically important traits, such as defense against parasitoids, within and among symbiont and animal host lineages.

Fig. 1

(A) Photograph of A. ervi parasitizing A. pisum. [Photo credit: Alex Wild] (B) Effect of APSE presence on the percentage of A. pisum successfully parasitized by the parasitoid wasp A. ervi. Aphid line 5A is uninfected with H. defensa, line A1A⁺ → 5A is the same A. pisum clone infected with H. defensa carrying bacteriophage APSE-3, and line A1A⁻ → 5A is the same A. pisum clone infected with the same strain of H. defensa but lacking phage APSE-3. (C) Effect of APSE on percentage of different A. pisum clonal lineages successfully parasitized by A. ervi. Numbers above columns refer to the total number of aphids counted as alive or parasitized. ***P < 0.0001.