One of the many problems farmers of various kinds of legumes need to deal with is the pea aphid, which reproduce incredibly fast and live by sucking the sap out of the plants. However, while they are terrifying parasites of legumes, they have their own yet more horrific parasites, a parasitoid wasp. Below is a really nice close up picture of one doing its thing, here is a video of the act, and here is a brain meltingly horrific video of a dissection of the mummified aftermath 8 days later. Essentially, these wasps deposit their eggs in a pea aphid and the growing larva feeds on it, developing there for about a week, and then consuming the host from the inside out like a Xenomorph. When it’s done, the wasp larva dries the aphid’s cuticle into a papery brittle shell and an adult wasp emerges from the aphid mummy. Legume farmers love these wasps as much as they despise the aphids that destroy their crops, however, when farmers noticed that the wasps didn’t work as effectively on all of aphids infestations, Nancy Moran’s group at the University of Texas in Austin went to work figuring out why. It turns out that all aphids have a primary bacterial endosymbiont living inside their cells, in addition to and much like a mitochondria, and that many have some combination of five other known secondary endosymbionts. Interestingly, two of those other five, Hamiltonella defensa and Serratia symbiotica have been shown to confer varying levels of resistance to the parasitoid wasp, allowing the aphid to survive infection. However, it turns out that there is yet one more layer to this story,
Big fleas have little fleas, Upon their backs to bite ’em, And little fleas have lesser fleas, and so, ad infinitum. And the great fleas, themselves, in turn Have greater fleas to go on; While these again have greater still, And greater still, and so on.
It is much like another wonderful paper, where a woman’s eye is a big flea bitten the smaller flea of an Acanthamoeba polyphaga parasite, which is in turn bitten by its Mimiviridae (Lentille virus), which is bitten by its virophage (Sputnik 2), which is itself in a sense bitten by its mobile genetic elements. We have a situation where the farmer is a big flea bitten by their legume, which is bitten by its aphid, which is then bitten by both its parasitoid wasp and its secondary endosymbiont, which is in turn then bitten by its temperate bacteriophage.
This post is deeply indebted to one made on Moselio Schaechter’s excellent blog Small Things Considered, which is slightly more technical and no doubt more clearly written.
Bacteriophages encode factors required for protection in a symbiotic mutualism
Oliver KM, Degnan PH, et al. Published 2009 in Science doi: 10.1126/science.1174463 [REQUIRES FREE REGISTRATION]
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.
The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes.
Moran NA, Degnan PH, et al. Published 2005 in PNAS USA, doi:10.1073/pnas.0507029102
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.