Unfortunately, we’ve got only journals in said lounge to keep me company, so I found myself thumbing through a recent issue of Science during my lunch break last week. I was understandably skeptical about the possibility of realizing any entertainment value within papers with titles such as “Adjoint Tomography of the Southern California Crust” (no offense, Geology). However, I was pleasantly surprised to stumble across a beguiling tale of mutualism run amok that I thought I’d share with you.
I should first admit that I’m a sucker for a good symbiosis story. Host meets parasite, parasite meets host, and two (or more) disparate species enter into an interpersonal relationship that sometimes leaves one or the other party the worse for wear. Mutualistic interactions (those in which each party benefits to some degree) abound, to be sure, but so do those in which one organism is essentially a selfish jerk. Some parasite jerks, such as the flea, are annoying at best, but some are downright diabolical.
The cuckoo bird provides a striking example of I-don’t-care-who-I-have-to-step-on parasitic behavior that would make Bernie Madoff blush. After a female cuckoo has mated, she scopes out the nest of a bird from a different species (for example, the reed warbler) and, while the unsuspecting warbler mom-to-be has her head turned, the cuckoo deposits her egg in the other’s nest, hoping the warbler failed counting in preschool and won’t notice that she now has five eggs instead of four. You might be surprised to hear that this risky gambit works relatively well – the unwitting foster parent will incubate the cuckoo egg as her own, and will even feed the nestling when it hatches, even if it looks very different from her own brood. In some cases, the cuckoo chick is larger than the foster mother! (<----- see?)To add a chilling twist to this wicked tale, some cuckoo chicks are programmed to have relatively short incubation times so that they’ll hatch before their foster siblings. Then, while the foster mother is out on the prowl, the cuckoo hatchling literally kicks the other non-cuckoo eggs out of the nest, slaying the genuine progeny of the foster bird (which have just plummeted to their untimely demise), so that he might be the sole recipient of the warbler’s able parenting. The “cuckolded” mommy, unaware of the cuckoo’s murderous behavior, dotes on the chick as if he were her own young, completely unaware that he most certainly is not. Indeed, the tragic story of the cuckoo brood parasite explains the etiology of the word “cuckold”, which refers to an unfortunate husband who unknowingly raises another man’s child as a consequence of his wife’s infidelity. Bummer.
Some symbiotic relationships, it turns out, involve multiple independent species and a complex network of mutualistic interactions. I recently became somewhat enamored of the perpetual struggle between the pea aphid (Acyrthosiphon pisum) and the parasitic wasp (Aphidius ervi), which has been chronicled at length in the scientific literature and serves as an elegant example of co-evolution in action. In short, the wasp reproduces by using the body of the aphid as an incubator for her fertilized eggs. The wasp quite literally injects her eggs into the aphid, which then develop inside of the living host. Then, in a grisly display, the larvae hatch and essentially eat their way out. This is probably not the sort of wasp you would trust to babysit your kids or repair your brakes. Fortunately for the aphid, it has evolved an independent symbiotic relationship with a bacterium that lives inside the aphid host and can be passed down from mother to child. It so happens that this bug, Hamiltonella defensa, is able to protect the aphid from wasp parasitism. That is, aphids with H. defensa “infections” survive even when wasps deposit their eggs – this is because the resident bacterium actually destroys the wasp embryos before they have a chance to develop and mature!
Despite the clear correlation between H. defensa infection and wasp resistance, the molecular underpinnings of this defense system were not immediately clear when this symbiosis was initially described. Much to my delight, a tantalizing new twist in the wasp-aphid-bacterium love triangle was reported in the issue of Science that I happened to pick up in my lab lounge during lunch (remember my burrito story?). University of Georgia entomologist Kerry Oliver and his colleagues at the University of Arizona recently showed1 that the genetic element within the bacterial endosymbiont that confers protection to the aphid from the wasp was in fact contributed by a fourth organism that had infected the bacterium! This new player is a member of the group we refer to as bacteriophages (“bacteria eaters”) - viruses that exclusively infect bacterial species.
As it turns out, the appropriately named bacteriophage A. pisum secondary endosymbiont (APSE) has itself formed a stable symbiosis with H. defensa via an old phage trick known as lysogeny. Lysogenic phages seamlessly and silently integrate their own genes into the genomes of their bacterial hosts. In so doing, the phage can essentially kick back, rest on its laurels, and have a few brewskies while the infected bacterium is left blissfully unaware that it is faithfully replicating the virus’ genetic material every time it replicates its own. Generations later, if the mood strikes, a lysogenic phage can choose to “go lytic” – that is, it can cut its genome back out of the host’s, build a swarm of new viral particles, and jump ship by bursting out of the cell that never realized it was there in the first place.
The upshot of the work of Oliver, et al is that the APSE phage is the actual agent responsible for protecting H. defensa-infected aphids from wasp parasitism. Whew! Let’s break this down, shall we?
Once the APSE phage has lysogenized its H. defensa host, not only will the bacterium replicate APSE’s genome free of charge, but it will also do the work of expressing some of the phage’s genes at no extra cost. In some cases, this can actually confer a benefit to the host by way of virulence.
For example, the brand of E. coli that is best known for causing foodborne illness and occasionally making spinach disappear from supermarket shelves is actually pathogenic because it has acquired toxins from a lysogenic phage called Stx. The Stx phage effectively "borrowed" a series of toxins from an entirely different species (Shigella dysenteriae) and then transferred them to E. coli upon infection and lysogeny. Put differently, the bacterium lets the phage crash at his place because the phage lent the bacterium a bazooka.
In the case of APSE, Oliver reports, the phage does the aphid a solid by arming H. defensa with a special arsenal of toxins that serve to attack the interloper wasp larvae.
Keep in mind that there are several complicated layers in the aphid-wasp-bacterium love triangle (now a love square, with the discovery of the phage). APSE is, after all, merely a parasite within a parasite – a stowaway within a stowaway. H. defensa infections are common among pea aphids, that’s true. However, Oliver is careful to point out that the arrangement between the aphid and its resident bacterium is only mutually beneficial when the parasitic wasp is around. In aphid subpopulations that are never exposed to the wasp, rates of H. defensa infection are significantly reduced. For the aphid, this likely means that it’s only worth letting the bacterium tag along with you when you need it to keep wasp babies from devouring you from the inside out. Over time, in the absence of wasp predation, aphids that aren’t harboring H. defensa seem to fare better than those that are still infected.
What’s more, those aphids that do hang on to the bacteria in the absence of wasp assaults have, in some cases, lost their immunity to wasp parasitism. When Oliver and colleagues kept H. defensa-infected aphids in a wasp-free environment for multiple generations and then exposed the progeny to wasps, some were vulnerable to the wasps even though they still harbored the endosymbiont bacterium. This is because the phage (which supplies the wasp-killing toxins) is often lost from the bacterial symbiont in the absence of selection (in this case, evil wasps), since, as the aphid came to appreciate with H. defensa, a parasite can surely overstay its welcome when it becomes no longer useful.
What is simply astonishing to me is the fact that the fate of a bacterial virus within a population of pea aphids is determined by the wasp, which is removed from the phage by three degrees of separation! The APSE phage is effectively shooed away by its bacterial host if it doesn’t need the viral toxins that prevent wasp larvae maturation in the aphid. The aphid, in turn, doesn’t need (or want) the bacterium if it can’t protect him from a gruesome wasp death or if there aren’t any wasps around in the first place. The enemy (APSE-infected H. defensa) of the aphid’s enemy (the wasp) is not quite a friend, since the aphid is clearly better off without any of those buggers in its body when it’s in a wasp-free environment. Still, the obvious advantage of keeping the bacterium and its stowaway around when wasps are about makes H. defensa the consummate “frenemy”. The aphid takes the bacterium, the bacterium takes the phage, the rat takes the cheese, the cheese stands alone.
I almost wish Hollywood would hastily put together a trite 75-minute PG-rated family movie based on this true story so that I would know whom to root for. I do sympathize with the plight of the aphid, which suffers a horrible fate at the hands of a winged bully (Boo, wasp!). However, the aphid has a nasty habit of destroying crops and other sorts of vegetation indiscriminately, and so has become the bane of many a farmer’s existence (Boo, aphid!). I don’t support using aphids as baby wasp factories, but I also don’t want them messing with my lettuce, especially when I’m hungry.
APSE is the hero of the day as far as the aphid and its bacterial endosymbiont are concerned. Of course, an APSE cousin did imbue an otherwise innocuous strain of E. coli with a more sinister worldview (along with the bacterial equivalent of weapons of mass destruction), and as much as I believe it’s unfair to hold the sins of the Stx phage against a certified wasp-killer, I still can’t in good conscience regale APSE with my version of “For He’s a Jolly Good Fellow”, even though I want to, if only because I do a pretty sick falsetto at the end part.
So, next time you find yourself in the lab lounge with your burrito surrounded by nothing but journals and vendor catalogues, find a random article and give it a read. It might surprise you, and you just might find (as I did) that sometimes there’s already more than enough drama in the natural world to keep you entertained on your lunch break.
1. Oliver, KM, et al, Science, 2009.
