Big fleas have little fleas, Upon their backs to bite ’em, And little fleas have lesser fleas, and so, ad infinitum.

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,

The relationship these endosymbionts have with the aphid, as well as the primary endosymbiont, is hard to classify as they confer a fitness cost in the absence of the wasp but a significant fitness boost when the wasps are around and trying to infect the aphids. At least for H. defensa, the reason why some strains are fully parasitic and provide no protection against the wasps while others are at least plausibly commensal and do provide protection, is a bacterial virus that infects the endosymbiont, even while it is inside the eukaryotic aphid cell. To understand why it will require a bit of knowledge of how some bacteriophages work. Most bacterial viruses, also known as bacteriophages, have a clear dividing line between two strategies. The simplest and most virulent phages will always immediately shut down their host’s metabolism upon infection and replace it with their own. Within a short period of time, generally between 20 and 80 minutes, the phage will have used the host cell to replicate its genome, build new viral particles, packed those particles with the genome and lysed the cell; setting loose 30-3000 new inert infectious particles. These are known as obligately lytic phages. Most phages however, use a mix of this strategy and another one known as lysogeny. These temperate phages will, at the beginning, decide to either virulently infect, producing particles at the total expense of the host, or hide in the host’s genome and inactivate all of its many host lethal genes. Generally it does this by expressing a transcriptional repressor that prevents expression of everything but the repressor, which incidentally protects the host from subsequent infection by related phages. However, some temperate phages will allow for expression of a genomic cassette that will perform some function of benefit to their host – they might as well since they are completely dependent on their host’s wellbeing while in this stage of their life cycle.
It turns out that there is a temperate bacteriophage called APSE, which is common in H. defensa populations in the aphids, that encodes for a cassette of genes that causes H. defensa to attack the wasp larvae with vicious toxins while the phage hides in the genome of its bacterial host. This makes for a really fascinatingly complex system of interdependencies for each of the agents involved. The phage, the bacterial symbiont, and the aphid are all each united in their interdependent need to combat the wasp that kills all three when it succeeds. However, at the same time, both the phage and the bacteria are dependent on the wasp to apply pressure on the aphid to keep them around – otherwise the aphid would cure itself of both creatures that would then be free-loading. Additionally, the wasp the bacteria, and the phage are all completely dependent on the aphid’s sap sucking ability to sustain them, and the aphid is totally dependent on the farmer to continue growing legumes in massive vulnerable monocultures. Furthermore the farmer and the legumes are dependent on the wasp to combat the aphid and largely helpless against the bacteria and the phage. At the same time, despite all of the interlocking incentives toward cooperation, there are also incentives towards each of these agents cheating each other. The farmer has an incentive to ‘cheat’ and save money by neglecting to buy aphid mummies every so often, because they still benefit from the fitness cost caused by the aphid not rejecting the bacteria or the bacteria rejecting the phage. Similarly, the aphid has an incentive to cheat both the bacteria and the phage to cure itself of them and bet on the farmer not buying aphid mummies full of wasps that year. The bacteria also has an incentive to cheat the aphid by curing itself of the phage, and also bet on the farmer not buying mummies that year itself.
What I love most about this story is that complex series of interdependent yet competing evolutionary interests, which forms as an emergent property of the Siphonaptera – this blog’s namesake,

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.

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One thought on “Big fleas have little fleas, Upon their backs to bite ’em, And little fleas have lesser fleas, and so, ad infinitum.

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