Of Ar­chaeal Periplasm & Icon­o­clasm

by Elio

Rough work, icon­o­clasm, but the only way to get at truth.
—Oliver Wen­dell Holmes

Bi­ol­ogy is the iconoclast's par­adise. Over and over, cher­ished be­liefs, some dat­ing back for cen­turies, fall to the ground as ex­cep­tions to the rule are dis­cov­ered. To the long list of such ex­cep­tions, we now add the find­ing by groups in Re­gens­burg and Frank­furt that the outer mem­brane of an ar­chaeon, Ig­nic­oc­cus hos­pi­talis, is en­er­gized and ca­pa­ble of gen­er­at­ing ATP. Granted, this is a hy­per­ther­mophile who helped shat­ter the an­cient be­lief that life at high tem­per­a­tures is not pos­si­ble, thus hardly a con­formist. But this dis­cov­ery is, to say the least, un­ex­pected.

A thin sec­tion of Ig­nic­oc­cus hos­pi­talis un­der the EM. C = cy­to­plasm. CM = "cyto­plasmic" mem­brane. P = periplasm. OS = outer sheath (mem­brane). Bar = 0.5 µm. Source

The old tenet is that the en­er­getic busi­ness-end of pro­karyotes is the cell mem­brane, whether sur­rounded by an outer mem­brane, as in Gram-neg­a­tives, or not, as in Gram-pos­i­tives. I should know, I taught this for umpteen years. True, in Gram-neg­a­tives, en­ergy can be transmit­ted to the outer mem­brane via the Ton sys­tem (a sys­tem that pro­vides en­ergy for the trans­port of iron siderophor­es, vi­t­a­min B12, and some col­icins), but the re­verse, mak­ing en­ergy on the outer mem­brane and send­ing it to the cy­to­plasm, is not part of the old be­lief. Yet it's been known for some time that a goodly num­ber of bac­te­ria can en­er­gize their outer mem­brane. They do this by hav­ing cyto­chro­mes in­serted in the outer mem­brane where they carry out a process known as ex­tra­cel­lu­lar elec­tron trans­fer. This abil­ity stands the or­gan­isms in good stead, al­low­ing them to uti­lize met­als in rocks as elec­tron ac­cep­tors.

Lo­cal­iza­tion of A₁A_o ATP syn­thase on I. hospi- talis cells in ul­tra­thin sec­tions. (A) La­bel­ing with an­ti­bod­ies against the pu­ri­fied AT­Pase com­plex, (B) La­bel­ing with an­ti­bod­ies against the mem­brane-bound sub­unit a. For both im­ages the sec­ondary an­ti­body with ul­tra­small gold par­ti­cles is vi­su­al­ized. C = cy­to­plasm. IM = in­ner mem­brane. V = vesi­cles in the pe­riplasm. OM = outer mem­brane. Source

First of all, dual mem­brane sys­tems have not be found in ar­chaea other than Ig­nic­oc­cus. What are the new conclu­sions about power gen­er­a­tion in its outer mem­brane based on? Mainly on im­mu­no­elec­tron mi­croscopy of sec­tions us­ing gold-la­beled an­ti­bod­ies and immunofluor­escence, which re­vealed that ATP syn­thase and H₂:sul­fur ox­i­dore­duc­tase are lo­cated en­tirely in the outer mem­brane. These two en­zymes are re­quired for en­er­giz­ing mem­branes and for ATP pro­duc­tion. Thus, ATP can be ex­pected be made in the outer mem­brane and re­leased into the periplasm (which in this or­gan­ism is huge – lar­ger than the cy­to­plasm). You may ask, are these two en­zymes also found in the in­ner mem­brane? The an­swer is no. Since the periplasm is so large and the two mem­branes so far apart, en­zyme lo­cal­iza­tion to one mem­brane or the other can be read­ily dis­cerned. This in­tro­duces the ques­tion: which is the cytoplas­mic mem­brane in this or­gan­ism? The fig­ure tells you some­thing about the rare struc­tural com­plexity of this or­gan­ism. Note that the two mem­brane sys­tem is dif­fer­ent from that of or­di­nary Gram-neg­a­tives, as here the outer mem­brane is not known to con­tain LPS or porins.

Co-cul­ture of Ig­nic­oc­cus spec. (green) and Nanoar­chaeum eq­ui­tans (red). ss rRNA se­quence-spe­cific flu­o­res­cence stain­ing. Bar = 1 µm. Source

Is the Ig­nic­oc­cus story rel­e­vant to other prokary­otes? Who's to say at this point. Ig­nic­oc­cus is might­ily idiosyn­cratic, e.g., it's unique among ar­chaea in hav­ing a two-mem­brane sys­tem. Not only does it grow at very high tem­per­a­ture and use re­duc­tion of el­e­men­tal sul­fur as its main en­ergy source, but it also lives in in­ti­mate asso­cia­tion with an­other ar­chaeon, the smaller Nanoar­chaeum eq­ui­tans, which has a re­duced genome and ap­par­ently gets its en­ergy from its larger part­ner. The un­usual ig­nicoccal abil­ity to make ATP within its periplasm may help it to sup­ply ATP to its as­so­ciates across the outer mem­brane.

The au­thors pro­pose a tan­ta­liz­ing no­tion: if the eukar­yotic cell arose by an ar­chaeon hav­ing swal­lowed a bac­terium (hold on, we're not get­ting into that dis­cus­sion right now), then Ig­nic­oc­cus or some­thing like it would have been the ideal an­ces­tor, able as it ap­pears to be to do­nate ATP to any­one re­sid­ing within its bound­aries. True or not, one should fur­ther re­spect the out­liers in the bi­o­log­i­cal scheme of things as po­ten­tial sources of novel and deeper re­la­tion­ships.

Ref­er­ence

Küper U, Meyer C, Müller V, Rachel R, & Hu­ber H (2010). En­er­gized outer mem­brane and spa­tial sep­a­ra­tion of meta­bolic processes in the hy­per­ther­mophilic Ar­chaeon Ig­nic­oc­cus hos­pi­talis. Pro­ceed­ings of the Na­tional Acad­emy of Sci­ences of the United States of Amer­ica, 107 (7), 3152–6 PMID: 20133662