Gul­liver and the Lil­liputians

by Elio & Merry

Two ar­chaea walk into a bar and the bar­tender says… No, we don't have an end­ing for this joke (tell us if you do!), but if the tem­per­a­ture of the bar were around 90°C and the lo­cal­ity a hy­drother­mal vent off Ice­land, there is a chance that the pair saun­ter­ing in could be one of the most in­ter­est­ing duos around. One part­ner is Ig­no­coc­cus hos­pi­talis, an ar­chaeon of re­spectable di­men­sions (2 μm di­am­e­ter) that is of­ten seen in close as­so­ci­a­tion with the much smaller Nanoar­chaeon eq­ui­tans.

"I found my arms and legs were strongly fas­tened on each side to the ground." Gul­liver's Trav­els, as illustrat­ed by Milo Win­ter.

To start with, the names of the or­gan­isms were cho­sen with care. Ig­no­coc­cus means "fiery coc­cus;" hos­pi­talis, "host;" eq­ui­tans, "horse rider." So, what about them?

I. hos­pi­talis is an anaer­o­bic chemolithotroph that gets its en­ergy from ox­i­diz­ing el­e­men­tal sul­fur us­ing mol­e­c­u­lar hy­drogen as the elec­tron donor. N. eq­ui­tans is tiny – ap­proximately 400 nm in di­am­e­ter – and has one of the small­est known genomes, some 490 kb. It lacks nearly all genes for lipid, co­fac­tor, amino acid, and nu­cleotide bio­synthesis. Not sur­pris­ingly, it can't be grown alone in the lab. It ob­tains its mem­brane lipids from its part­ner, and likely its amino acids, as well. For more in­ti­mate de­tails, see a new re­port in the Jour­nal of Bac­te­ri­ol­ogy that de­scribes an in­ter­est­ing col­lec­tion of phys­i­o­log­i­cal and struc­tural stud­ies.

One would ex­pect such a drain of re­sources to have some neg­a­tive im­pact on the host cells, but in the lab I. hos­pi­talis grows just as well with or with­out its part­ner. Its dou­bling time is not re­duced, and nei­ther is the fi­nal cell den­sity. How­ever, some­thing is go­ing on. Dur­ing ex­po­nen­tial growth in co-cul­tures, about a third of the Ig­no­coc­cus cells are seen to carry 2–3 N. eq­ui­tans cells. When en­tering the sta­tion­ary phase, most Ig­no­coc­cus cells are cov­ered with as many as ten N. eq­ui­tans, re­mind­ing us of Gul­liver out­num­bered and over­run by Lil­liputians. On the other hand, N. eq­ui­tans does not pro­lif­er­ate un­til the host en­ters sta­tion­ary phase. Who's in­hibit­ing whom? This sounds com­pli­cated. The au­thors sug­gest:"…that the as­so­ci­a­tion of I. hos­pi­talis and N. eq­ui­tans repre­sents a highly spe­cial­ized sys­tem. Con­se­quently, as­sign­ment to the clas­si­cal cat­e­gory of sym­bio­sis, com­men­sal­ism, or par­a­sitism might not be pos­si­ble even in the fu­ture."

TEM of ul­tra­thin sec­tions of I. hos­pi­talis and N. eq­ui­tans fol­low­ing cryopro­cessing. CM, cy­to­plas­mic mem­brane; OM, outer mem­brane; Pp, periplasm; PV, periplas­mic vesi­cles. White ar­rows point to the con­tact site where the I. hos­pi­talis outer mem­brane is in close con­tact with the cy­to­plas­mic mem­brane. Bars, 1 µm. Source

But N. eq­ui­tans has other unique traits that are both ex­traordinary and in­trigu­ing. Phy­lo­ge­net­i­cally, it is a thing onto it­self. For starters, it is the only char­ac­ter­ized mem­ber of the king­dom Nanoar­chaeota, a group thought to rep­re­sent a very an­cient branch of the tree of life, maybe go­ing all the way back to the be­gin­ning (the pre­cise branch­ing point be­ing still un­der de­bate.) Its diminu­tive genome pos­sesses unique and po­ten­tially an­cient an­cestral traits. Five of its tR­NAs are en­coded by genes that are split along the genome. The RNAs are later spliced to­gether. Nowhere else does one find this way of mak­ing tR­NAs. In all cases, the split oc­curs at a site ad­ja­cent to the an­ti­codon – the nor­mal lo­ca­tion for tRNA in­trons. One is prompted to won­der about the why and the how of this trans splic­ing mech­a­nism, as well as to spec­u­late about the evo­lu­tion­ary ori­gins of tR­NAs. (For the lat­est, click here.) There are nu­mer­ous pro­tein-en­cod­ing genes that are split, too. And un­like other Ar­chaea, this or­gan­ism lacks oper­ons. Not that it lacks the genes, but in­stead of be­ing clus­tered, they are scat­tered about the genome.

An­other dis­tin­guish­ing fea­ture is that N. eq­ui­tans is ar­guably the best, al­though per­haps not the only, ex­am­ple of a par­a­sitic ar­chaeon. Why the Ar­chaea have not ex­hib­ited greater gusto for a par­a­sitic lifestyle is an open ques­tion.