The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes

TLDR

Aphids harbor complex mutualistic consortia of coinherited bacteria, with the primary endosymbiont Buchnera supplying essential nutrients and secondary symbionts such as Hamiltonella defensa providing defense against natural enemies, yet genomic analysis of these uncultivable secondary symbionts has been hampered by DNA isolation challenges. The study proposes that phage‑borne toxin genes in Hamiltonella defensa confer protective benefits to aphids against eukaryotic parasites. The authors amplified hemolymph DNA from infected pea aphids to sequence Hamiltonella defensa and its APSE‑2 bacteriophage, revealing that H. defensa carries two type III secretion systems and that APSE‑2 encodes a cytolethal distending toxin homolog capable of disrupting eukaryotic cell cycles.

Abstract

Aphids maintain mutualistic symbioses involving consortia of coinherited organisms. All possess a primary endosymbiont, Buchnera , which compensates for dietary deficiencies; many also contain secondary symbionts, such as Hamiltonella defensa , which confers defense against natural enemies. Genome sequences of uncultivable secondary symbionts have been refractory to analysis due to the difficulties of isolating adequate DNA samples. By amplifying DNA from hemolymph of infected pea aphids, we obtained a set of genomic sequences of H. defensa and an associated bacteriophage. H. defensa harbors two type III secretion systems, related to those that mediate host cell entry by enteric pathogens. The phage, called APSE-2, is a close relative of the previously sequenced APSE-1 but contains intact homologs of the gene encoding cytolethal distending toxin ( cdtB ), which interrupts the eukaryotic cell cycle and which is known from a variety of mammalian pathogens. The cdtB homolog is highly expressed, and its genomic position corresponds to that of a homolog of stx (encoding Shiga-toxin) within APSE-1. APSE-2 genomes were consistently abundant in infected pea aphids, and related phages were found in all tested isolates of H. defensa , from numerous insect species. Based on their ubiquity and abundance, these phages appear to be an obligate component of the H. defensa life cycle. We propose that, in these mutualistic symbionts, phage-borne toxin genes provide defense to the aphid host and are a basis for the observed protection against eukaryotic parasites.