When I am exposed to mystery rays from outer space and develop superpowers, I want it to involve a symbiotic virus that I can use to attack my foes. I swear that I will use this power only for good. 1
Of course, I’ve been beaten to the big cartoon punch. When I first heard about polydnaviruses, about ten years ago, I realized that I could never be as cool as a microgastroid wasp.2 Microgastrinae and Campopleginae are parasitoid wasps that have (apparently independently) managed to set up a spectacular symbiotic relationship with polydnaviruses. The wasps are predators of other insects; they lay their eggs on caterpillars or aphids or whatever, the eggs hatch, and the wasp larvae eat their host from the inside out, finally emerging as new adult wasps.
Understandably, the host caterpillar is not all that enthusiastic about this process, and attempts to defend themselves with an immune response to the wasp larvae. In an effective immune response against endoparasitoids, the host’s immune cells (hemocytes) will encapsulate the parasite, wrapping it up and walling it off from the host. 3 Successful parasitic wasps (of which there are a huge number; this is a very popular ecological niche) must avoid their dinner’s immune system, and there are many different routes to to this goal.
Now hold that thought for a moment while I change the subject to viruses. One characteristic of a successful virus is that it must, to some extent, avoid its host immune system. I’ve talked about that in mammalian viruses , and insect viruses are in principle no different. Insects don’t have an adaptive immune system (though see some discussion of that here and here), and insect viruses therefore have to deal with mechanisms like recognition and encapisidation by hemocytes.
4 wasps set up a symbiosis with viral pathogens of the wasps’ prey. The wasps use the virus’s immune evasion functions — of which there are a huge number5 and which, as well as being interesting in their own right, have obvious potential uses in pest control — to avoid elimination by their host’s immune system. And what do the viruses get out of it? They get free replication out of it: They’ve become completely integrated into the wasp genome. They’re no longer a free-living6 entity; they do not replicate in the cells of the host, nor do they replicate independently in the wasp cells. The only way the viral genome can make a new viral genome is in the genome of the wasp that they are helping parasitize a new host.You see where this is going. Some 75 million years ago,
The symbiosis model is the traditional explanation, but it’s not the only one. There are at least two, probably three, and maybe more, lineages of polydnavirus-carrying wasps, and the polydnavirus sequences seem to be very different, suggesting that the wasp lineages arose independently. For some of these, there is at least some evidence that the polydnaviruses arose from free-living viruses;7 but for other it’s been suggested that the polydnaviruses actually represent expansion of wasp genes that then grabbed a capsid protein and became virus-like after the fact: 8
A more parsimonious hypothesis would be that bracoviruses do not originate from any of the large genome viruses characterized to date. They may have been built up from a simple system producing circular DNA intermediates, such as mobile elements, within the wasp genome. The acquisition of a capsid protein, possibly of viral origin, around the circular DNA intermediates would have allowed infection of lepidopteran cells. Finally, virulence genes could have been acquired from the wasp genome at different times during evolution of bracovirus-bearing wasp lineages, thus explaining why CcBV genes encoding proteins with a predicted function resemble cellular genes.
In any case, this approach has turned out to be incredibly successful, with tens of thousands of parasitic wasps making use of these bioweapons.
- Although, you know that guy with the hat? With his blinker on, driving 45 mph in the fast lane? PEW! PEW! PEW![↩]
- Or, for that matter, as a campoplegid wasp.[↩]
- A nice review of the insect immune response to endoparasitoids is Schmidt O, Theopold U, Strand M. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays. 2001 ;23(4):344-351.[↩]
- Whitfield, J.B. Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc Natl Acad Sci U S A 99, 7508-7513 (2002).[↩]
- Recent examples include — Beck, M.H. & Strand, M.R. A novel polydnavirus protein inhibits the insect prophenoloxidase activation pathway. Proc Natl Acad Sci U S A doi:10.1073/pnas.0708056104 (2007).
Thoetkiattikul, H., Beck, M.H. & Strand, M.R. Inhibitor kappaB-like proteins from a polydnavirus inhibit NF-kappaB activation and suppress the insect immune response. Proc Natl Acad Sci U S A 102, 11426-11431 (2005). [↩]
- to the extent any virus can be free living[↩]
- 1. Lapointe, R. et al. Genomic and Morphological Features of a Banchine Polydnavirus: Comparison with Bracoviruses and Ichnoviruses. The Journal of Virology 81, 6491-6501 (2007).[↩]
- Espagne, E. et al. Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306, 286-289 (2004).[↩]