Book Re­view: Viruses – Es­sen­tial Agents of Life

by Welkin John­son

Vi­rol­ogy was born in 1898, and has suf­fered from sam­pling bias ever since. For decades, viruses were de­fined by what they were not: not as big as a bac­terium, not vis­i­ble with a mi­cro­scope, not cul­tur­able in the ab­sence of a host. At the dawn of the 20th cen­tury, undis­cov­ered viruses and as­pir­ing Hol­ly­wood star­lets had the same challenge—how to catch someone's at­ten­tion. Thus, the first viruses known to sci­ence were those caus­ing very ob­vi­ous phe­no­types in clin­i­cally or agri­cul­tur­ally im­por­tant hosts: yel­low fever in hu­mans, mo­saic dis­ease in to­bacco, foot-and-mouth dis­ease in live­stock. The acid-test was the abil­ity to pass through the pores of a Cham­ber­land or Berke­feld fil­ter; the viruses that were eas­i­est to find were those that pro­duce in­fec­tious cell-free virions—another source of dis­cov­ery bias. And, in the days be­fore cell cul­ture, the eas­i­est of those to study were the ones that in­duced rapid and ob­vi­ous patho­gen­e­sis in a con­ve­niently avail­able host or­gan­ism. By mid-20th cen­tury, tech­nol­ogy fos­tered the move to re­duc­tion­ist ex­per­i­men­ta­tion, in­clud­ing elec­tron mi­croscopy, X‑ray crys­tal­log­ra­phy, cell-cul­ture and, of course, re­com­bi­nant DNA tech­nol­ogy. Vi­rol­o­gists moved into lab­o­ra­to­ries, and the model sys­tems they chose to bring with them were of­ten those al­ready in place, proven to be tractable and con­sid­ered rel­e­vant by fund­ing agen­cies. To­day you can pe­ruse any vi­rol­ogy text­book and get the im­pres­sion that less than two dozen viruses rep­re­sent the en­tirety of Earth's vi­ros­phere.

Viruses: Es­sen­tial Agents of Life (2012, Springer), edited by Gün­ter Witzany, is a great way to kick off the next 100 years of vi­rol­ogy, with nary a re­duc­tion­ist thought to be found within its 427 pages. This is not a com­pendium of re­view ar­ti­cles, and stu­dents seek­ing an­swers to ar­cane ques­tions posed by aloof pro­fes­sors will be frus­trated if they think they will find those an­swers here. What they will find, in abun­dance, are thought-pro­vok­ing ideas of the "bigc­ture" va­ri­ety (with a bit of con­tro­versy and philo­soph­i­cal de­bate thrown in for good mea­sure). Most im­por­tantly, read­ers will find many ex­cit­ing rea­sons to be a vi­rol­o­gist (am­a­teur or pro­fes­sional) at the dawn of the 21st cen­tury.

We've learned a lot about how viruses work since 1898, and now, as vi­rol­ogy en­ters its sec­ond cen­tury, vi­rol­o­gists are in­creas­ingly cu­ri­ous about viruses in na­ture. The sheer abun­dance of viruses on Planet Earth is start­ing to sink in, and ques­tions abound: how do viruses evolve in na­ture, in pop­u­la­tions, and in out-bred hosts oc­cu­py­ing all ex­tremes and all pos­si­ble en­vi­ron­men­tal niches? Were viruses present dur­ing the ori­gins of life, and if so, what role did they play? Given the im­men­sity of the vi­ros­phere, it is not a ques­tion of if but how viruses have dri­ven or­gan­is­mal evo­lu­tion since the days of LUCA. Viruses are every­where and in abun­dance, and the time has come to sit up and take no­tice. Viruses: Es­sen­tial Agents of Life helps point the way.

The top­ics dis­cussed range widely across vi­rol­ogy, with chap­ters on the roles of viruses in form­ing new genes; gi­ant viruses; plant viruses; spillover in­fec­tions; viruses and the ori­gins of life; eye-pop­ping cal­cu­la­tions of the size and scope of the vi­ros­phere; sep­a­rate chap­ters on retro­viruses in the process of in­vad­ing the germlines of sheep and koalas; and the po­ten­tial for virus struc­ture to as­sist with re­con­struct­ing deep evo­lu­tion­ary con­nec­tions be­tween viruses (in­clud­ing viruses hail­ing from the three dif­fer­ent do­mains of life). There is a quar­tet of chap­ters in­spired by the re­cent dis­cov­ery of gi­ant viruses (e.g., Mimivirus), each ex­plor­ing a dif­fer­ent theme, at times even dis­agree­ing with one an­other. Jean-Michel Claverie and Chan­tal Abergel re­visit an ear­lier era of virus-in­spired phi­los­o­phy, care­fully re­con­sid­er­ing An­dre Lwoff's con­cept of the virus point-by-point in light of Mimivirus and its cousins.

A re­cur­ring theme in the book is the no­tion that viruses are more than par­a­sites en­gaged in cycli­cal preda­tor-prey re­la­tion­ships with their hosts. Mar­i­lyn Rooss­inck sug­gests that the fo­cus on viruses as agents of dis­ease has led to a bias in our un­der­stand­ing of viruses in na­ture, that we ig­nore "the prob­a­bil­ity that viruses may play im­por­tant roles in the ecol­ogy of their hosts [ital­ics are mine]." She points to the gen­er­a­tionally-sta­ble, per­sis­tent en­dor­naviruses of plants as a likely source of sym­bioses, and fur­ther sug­gests that such re­la­tion­ships will largely be over­looked if we fo­cus only on model or­gan­isms in ex­per­i­men­tal settings—in other words, viruses may take on un­ex­pected roles within the ecosys­tems of their hosts.

Luis Vil­lareal, one of the most con­sis­tently thought-pro­vok­ing vi­rol­o­gist-writ­ers I know, also urges us to re­con­sider our no­tion of virus-host re­la­tion­ships, ar­gu­ing for ex­am­ple, that en­demic in­fec­tion it­self may be a se­lec­table phe­no­type of the host pop­u­la­tion, and sug­gest­ing that study­ing any or­gan­ism in the ab­sence of its viruses is mis­lead­ing: "In­deed … it is the prod­ucts of viruses (such as trans­posases or cap­sids) that are the most preva­lent genes in na­ture … the im­pli­ca­tions of the mas­sive om­nipres­ence can no longer be ig­nored."

Ni­pah virus. Source

Among my fa­vorite con­tri­bu­tions is a chap­ter on bat viruses, eco­log­i­cal change and spillover in­fec­tions, con­tributed by Har­ald Brüs­sow. Brüs­sow uses top-notch sto­ry­telling and a hint of au­to­bi­og­ra­phy to cre­ate a lively es­say in the time-hon­ored tra­di­tion of Mon­taigne. He retells sev­eral "de­tec­tive sto­ries", track­ing out­breaks of Hen­dra virus, Ni­pah virus, Ebola virus and the SARS coro­n­avirus, among oth­ers, and re­lat­ing these to the op­por­tu­ni­ties for cross-species trans­mis­sions cre­ated by eco­log­i­cal change. Im­por­tantly, and in keep­ing with the theme of the book, Brüs­sow en­gages in provoca­tive spec­u­la­tion about the ad­van­tages these viruses may sup­ply to their nat­ural chi­ropteran hosts when­ever other or­gan­isms in­vade their space (pre­cisely the sit­u­a­tion cre­ated by hu­man in­cur­sions into bat ter­ri­tory).

Some read­ers will read this book from front to back. Oth­ers, like me, are likely to jump around like ex­cited chil­dren in a toy store. For the lat­ter, I rec­om­mend be­gin­ning with the aptly named "Scratch­ing the Sur­face of Biology's Dark Mat­ter", by Merry Youle, Matthew Haynes and For­est Ro­hwer. You can't tell the play­ers with­out a pro­gram, and as it turns out, there are a lot of players—as in "1" fol­lowed by a few dozen ze­ros. Even if the es­ti­mates of global vi­ral abun­dance and di­ver­sity pre­sented by Youle, Haynes and Ro­hwer are off by sev­eral or­ders of mag­ni­tude, they are still sev­eral or­ders of mag­ni­tude be­yond hu­man com­pre­hen­sion! More im­por­tant than the ac­cu­racy of these num­bers, how­ever, is the in­escapable fact that viruses are ma­jor pur­vey­ors of ge­netic novelty—the pri­mary theme of the chap­ter. Any­one who is wor­ried that there is noth­ing new un­der the sun should start here.

Sins of omis­sion will oc­cur to some read­ers. The lack of a chap­ter on the in­cip­i­ent field of pa­le­ovi­rol­ogy is a glar­ing one, in my opin­ion. In par­tic­u­lar, the re­cent dis­cov­ery that all kinds of viruses (not just retro­viruses) leave mol­e­c­u­lar "fos­sils" de­posited in the ge­nomic strata of their hosts would have fit nicely in this book, ex­tend­ing the study of vi­ral di­ver­sity to em­brace the tem­po­ral di­men­sion, call­ing into ques­tion com­mon as­sump­tions used to in­fer his­tory with phy­lo­ge­netic meth­ods, and in­form­ing our un­der­stand­ing of how viruses in­flu­ence the evo­lu­tion of liv­ing or­gan­isms.

Viruses: Es­sen­tial Agents of Life was not edited for con­sis­tency of style, which, no doubt, would have been a dif­fi­cult task given al­most fifty au­thors and co-au­thors writ­ing from at least nine coun­tries! Chap­ters range from nine to thirty-eight pages in length, with very lit­tle at­ten­tion paid to spelling, gram­mar or syn­tax.  All of this makes read­ing the book from be­gin­ning to end a bit rough go­ing, and for some, this may be off-putting. Hope­fully, most read­ers will stick with it, be­cause every sin­gle chap­ter is rich in ideas. And for me, the rough edges had the pleas­ant ef­fect of evok­ing the ver­nac­u­lar of con­ver­sa­tion (rather than the au­thor­i­ta­tive, pas­sive voice be­hind which sci­en­tists when writ­ing typ­i­cally hide).  Read­ing this book was like eaves­drop­ping on a heated con­ver­sa­tion among the au­thors, as if I'd dropped into an in­ter­con­ti­nen­tal pub for a pint and an evening of im­pas­sioned, free-rang­ing de­bate about viruses and the mean­ing of life.

Note:  If you have ac­cess to e‑journals and sim­i­lar ma­te­ri­als, you may be able to down­load the en­tire book in PDF for­mat from Springer here.

Welkin John­son is on the fac­ulty of Boston Col­lege and an as­so­ciate blog­ger of Small Things Con­sid­ered.