Sex­u­ally Avoided Dis­ease

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 dy–namics, 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.

Fig­ure 1. True color satel­lite im­age of a mil­ky E. hux­leyi bloom in the Eng­lish Chan­nel, south of Ply­mouth, UK, on 30 July 1999. This bloom was ef­fec­tively 'dead' and up to 1 mil­lion E. hux­leyi-spe­cific coc­col­ithoviruses per tea­spoon of wa­ter were found in the mid­dle of the high-re­flectance wa­ter. Cour­tesy of the Ply­mouth Ma­rine Lab­o­ra­tory Re­mote Sen­sing Group

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.

Fig­ure 2. Virus (ap­prox. 190 nm di­am­e­ter) at­tached to a coc­col­ith from an E. hux­leyi cell. Source

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.