A Happy Hot Cou­ple

by Elio

We don't know about you, but we've be­come pretty blase about the stream of pa­pers, each with the cus­tom­ary two dozen or more au­thors, re­port­ing the com­pleted genome of yet an­other mi­crobe. But the re­cent one on the ar­­chae­on Ig­nic­oc­cus hos­pi­talis mer­its spe­cial at­ten­tion. Com­bined with the pre­vi­ously se­quenced genome of Na­noarchaeum eq­ui­tans, we have a ge­nomic win­dow into one of the most ex­cit­ing sym­bioses in the mi­cro­bial world. We pre­vi­ously vis­ited with this pair, and re­turn now to con­tinue their story.

The south­ern end of the vol­canic Kol­bein­sey Ridge with its iso­lated sea­mounts perched on the Mid-At­lantic rid­ge north of Ice­land. Source

This ar­chaeal duo make up the only known oblig­a­tory ec­tosymbiosis among prokary­otes. There are sym­bioses aplenty be­tween and among Bac­te­ria and Ar­chaea within the pro­fu­sion of mi­cro­bial com­mu­ni­ties on our planet. But in all those other cases, the part­ners have a some­what ca­sual phys­i­cal as­so­ci­a­tion. Re­sid­ing within multi­layered biofilms or ag­gre­gates, meta­bolic part­ners might not even be touch­ing. Here, the two are in in­ti­mate con­tact. One, the tiny N. eq­ui­tans, re­quires its I. hos­pi­talis "host" for sur­vival – thus meet­ing the de­f­i­n­i­tion of oblig­a­tory.

They were both dis­cov­ered (re­ported here and here) by Karl Stetter's group in hy­drother­mal vents north of Ice­land. Both are hy­per­ther­mophiles, thriv­ing at around 90 °C. Ig­nic­oc­cus hos­pi­talis ("hos­pitable fire sphere") is a mem­ber of the Desul­furo­coc­cales, a re­spectable or­der within the phy­lum Cre­nar­chaeota. It has the dis­tinc­tion of be­ing the only known oblig­a­tory anaer­o­bic sul­fur-re­duc­ing chemolithoau­totroph in that group. Ig­nic­occi fix CO₂ by a novel path­way in which acetyl-coen­zyme A serves as the pri­mary CO₂ ac­cep­tor; they get en­ergy from sul­fur re­duc­tion us­ing hy­dro­gen as the elec­tron donor. On the other hand, N. eq­ui­tans ("the rid­ing dwarf") be­longs to an in­trigu­ing, deeply branch­ing ar­chaeal phy­lum, the Nanoar­chaeota. Whether its nu­mer­ous unique prop­er­ties are ex­tremely an­cient or highly de­gen­er­ated re­mains an open ques­tion so far.

a) TEM Freeze etch­ing of an I. hos­pi­talis cell with four at­tached N. equi­tans cells. b) TEM ul­tra­thin sec­tion of two N. eq­ui­tans, at­tached to the outer mem­brane of an Ig­nic­oc­cus. c) I. hos­pi­talis with sev­eral N. eq­ui­tans cells. CLSM Con­fo­cal mi­croscopy of co-cul­ture of N. eq­ui­tans (red) and I. hos­pi­talis (green) af­ter se­quence spe­cific (ss rRNA) fluor­escence stain­ing. Bars: 1 µm. Source

Nanoar­chaea are "nano" in­deed, only 400 nm in diame­ter – about 5% of the vol­ume of your ar­che­typ­i­cal 1 μm³ prokary­ote. It's been known for some time that N. equi­tans has a puny genome, barely 490 kbp, be­low what may be the thresh­old genome size re­quired for liv­ing freely. It lacks genes for a whole slew of the usual me­tabolic biosyn­thetic en­zymes. In­deed, it has been shown that lipids, and most likely many other metabo­lites, are trans­ferred from Ig­nic­oc­cus to the nanoar­chaeon rider. Not that Ig­nic­oc­cus is so well en­dowed ei­ther. Its scant 1.3 Mb genome lacks a lot of the me­tab­o­lism-re­lated genes found in the other, typ­i­cally het­erotrophic, Cren­archaeota. (No, those miss­ing genes are not pro­vided by the rid­ers.)

It's easy to see what the nanoar­chaeon gets out of this part­ner­ship, but what ben­e­fits ac­crue to the host Ig­nic­oc­cus? Not known. Not only can it grow with­out its part­ner, but its growth seems at times hin­dered by car­ry­ing the nanoar­chaea. But surely there is more to it. The hy­drother­mal vents are not only a hot place, which seems to suit these two or­gan­isms just fine (liv­ing at high tem­per­a­tures is just an­other day at the of­fice for them), but they are also highly tur­bu­lent. No tran­quil en­vi­ron­ment this. How the two part­ners find each other to es­tab­lish the sym­bio­sis is a good ques­tion. Nanoar­chaea have re­cently been re­ported from other habi­tats, in­clud­ing mesophilic and halophilic ones, so, who knows!

3D re­con­struc­tion based on a se­ries of ul­tra­thin sec­tions. White ar­rows point to pe­riplasmic vesi­cles. Purple/rose cyto­plasmic mem­brane. Bar: 1 μm. Source

Ques­tions arise as to how the needed metabo­lites are trans­ferred from host to rider. Both species lack the me­chanisms that would al­low di­rect trans­port from cell to cell. Like­wise, var­i­ous con­straints limit what could be se­creted by the Ig­nic­oc­cus. But ig­nic­occi and nanoar­chaea have a rar­ity among the Ar­chaea, a dou­ble mem­brane sys­tem sep­a­rated by a periplas­mic space. Not only that, but the ig­nic­occi pos­sess the mother of all periplasms, some­times oc­cu­py­ing half the vol­ume of the cell.

Re­cent 3D re­con­struc­tions of the cell-cell con­tact re­gion sug­gest that mul­ti­ple mech­a­nisms may be at work here. There is rea­son to be­lieve that the ig­nic­occi bud off ve­sicles from their cy­to­plas­mic mem­brane and that these travel to the outer mem­brane, there to fuse with the mem­brane of the nanoar­chaeon.

Con­tact sites of I. hos­pi­talis with cells of N. eq­ui­tans in ul­tra­thin sec­tion. Bar: 200 nm. Source

The pa­per an­a­lyz­ing the genome of I. hos­pi­talis has thor­ough dis­cus­sion of the roles of most of its genes, with in­ter­est­ing notes about gene ac­qui­si­tion and ge­nome re­duc­tion. It makes very good read­ing, es­pe­cially for afi­ciona­dos of meta­bolic an­no­ta­tions. Ar­chaea are full of sur­prises, as would be ex­pected from or­gan­isms with such ex­treme sur­vival tal­ents. It's not hard to be­lieve that many more are in store.

We once prompted: Two ar­chaea walk into a bar… and Fred Rosen­berg replied: …and the bar­tender said, "Woese is me!"