by Willie Wilson
The Red Queen’s race in Lewis Carroll’s Alice in Wonderland is a common metaphor for an evolutionary arms race. A good example can be seen in predator-prey dynamics, particularly virus-host interactions where hosts must rapidly evolve immunity to infection for survival of the species. It takes all the running you can do to stay in the same place.
Red Queen dynamics can also help explain the bloom-bust cycles of oceanic algae that can be seen readily from space in satellite images. One such alga is Emiliania huxleyi, a 5 µm diameter eukaryotic cell that has an elaborate armory of calcareous coccoliths. It is ubiquitous in the world’s oceans and forms dense milky blooms that cover vast areas of mainly temperate oceans. Until recently, the mechanisms of E. huxleyi bloom disintegration were poorly understood, but it is now accepted that viruses (referred to as coccolithoviruses) are intrinsically linked to these sudden crashes.
A recent report describes a novel sex strategy that E. huxleyi has adopted to avoid coccolithovirus infection. The team thinks the solution is so incredible they have dubbed it the ‘Cheshire Cat’ escape strategy, after the disappearing antics of another famous character in Lewis Carroll’s book. The microalga responds to coccolithovirus attack by switching from its usual diploid life stage (where it is susceptible to infection) to a haploid cell, essentially changing its physical appearance, making it impenetrable to the deadly coccolithovirus. As diploids, E. huxleyi are non-motile coccolith-bearing cells, perhaps ironic given some early thinking that coccoliths actually played an antiviral role. The motile flagellated haploid cells lose their chalk armory and are instead covered by organic scales which may be the mechanism of resistance by acting as a physical barrier.
It is a clever antiviral strategy and will create a reservoir of resistant haploid cells that can have sex and possibly create a huge variety of new E. huxleyi genotypes. Eventually, some of the fitter genotypes will succeed in generating new blooms when the environmental conditions are favorable. This constantly changing genetic landscape in response to coccolithovirus infection will be critical in buffering the effects of rapid climate change, such microorganisms will be the first to react and adapt to a changing ocean. Selection for sexual reproduction as an antiviral mechanism will also maintain a high diversity ensuring that there will always be a genetic variant that can adapt to a particular environmental condition.
With the synergistic effect of chemical warfare and selective grazing of coccolithovirus infected cells you almost start feeling sorry for the E. huxleyi-specific coccolithoviruses with so many systematic antiviral mechanisms in place. However, with such an ancient evolutionary origin and a huge genome of novel and unknown genes, it is likely the coccolithoviruses have a barrage of equally clever counter-intelligence strategies to ensure the coccolithoviruses are ultimately the victors. Clearly it is part of a complex evolutionary arms race that Red Queen and now Cheshire Cat hypotheses are trying to epitomize, but as a marine virologist, I like to think the coccolithoviruses have the upper edge!
Willie Wilson is Senior Research Scientist at Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, Maine. An authority on marine viruses, he is an author of numerous reports in this field, including this one, this one, and this one.