Cul­ti­vat­ing the An­ces­tors… (2|4)

by Christoph

A model for eu­karyo­ge­n­e­sis

Based on their knowl­edge of the mor­phol­ogy of P. syn­troph­icum MK-D1 from elec­tron micro­scopy and their knowl­edge of its phys­i­ol­ogy from growth as­says and genome analy­sis, Imachi, Nobu et al. (2020) pro­pose a hy­po­thet­i­cal model, the E3 model, of how the first evolution­ary steps to­wards eu­karyo­ge­n­e­sis might have oc­curred in an an­ces­tral ar­chaeon liv­ing ~2 bil­lion years ago. I quote their com­ments on Fig­ure 3 ver­ba­tim, with my re­marks in square brack­etts:

Fig­ure 3. Pro­posed hy­po­thet­i­cal model for eukar­yo­ge­ne­sis (E3). See text for de­tails. Mod­i­fied from Source. Fron­tispiece: Promet­hearchaeum syntrophi­cum MK-D1. Scale bar, 500 nm. Source

a  The syntrophic/fermentative host ar­chaeon ['As­gard' branch] is sug­gested to de­grade amino acids to short-chain fatty acids and hy­dro­gen (H2), pos­si­bly by in­ter­act­ing with H2-scav­eng­ing (and in­di­rectly O2-scav­eng­ing) sul­fate-re­duc­ing bac­te­ria (SRB) (or­ange).

b  The host may have fur­ther inter­acted [during/after the Great Ox­i­da­tion Event (GOE)] with a fac­ul­ta­tively aer­o­bic organ­otrophic part­ner that could scav­enge toxic O2 (the fu­ture mitochon­drion; red). Con­tin­ued in­ter­ac­tion with SRB could have been ben­e­fi­cial but not nec­es­sar­ily es­sential; dot­ted ar­rows in­di­cate the inter­action.

c  Host ex­ternal struc­tures [blebs, pro­tru­sions] could have in­ter­acted (for ex­am­ple, me­chan­i­cal or bi­o­log­i­cal fu­sion) with the aer­o­bic part­ner to en­hance phys­i­cal in­ter­ac­tion and fur­ther en­gulf the part­ner for si­mul­ta­ne­ous de­velopment of en­dosym­bio­sis and a prim­i­tive nu­cleoid-bound­ing mem­brane.

d  Af­ter en­gulf­ment, the host and sym­biont could have con­tin­ued the in­ter­ac­tion shown in b as a prim­i­tive type of endosym­biosis.

e  De­vel­op­ment of ADP/ATP car­rier (AAC) by the en­dosym­biont (the ini­tial di­rec­tion of ATP trans­port re­mains un­clear).

f  En­do­g­e­niza­tion of part­ner sym­bio­sis by the host through del­e­ga­tion of ca­tab­o­lism and ATP gen­er­a­tion to the en­dosym­biont and es­tab­lish­ment of a sym­biont-to-host ATP chan­nel.

Note  Masaru Nobu ex­plained the E3 model in more de­tail than I can here in his recorded contri­bu­tion to the JGI2021 Meet­ing.

An­other model for eu­karyo­ge­n­e­sis

Older mod­els of eu­karyo­ge­n­e­sis posited that evolv­ing the ca­pa­bil­ity for en­do­cy­to­sis was a pre­req­ui­site for the up­take of a (fu­ture) mi­to­chon­drion by the prog­en­i­tor of the eu­kary­otic cell (Out­side-in Model(s)). This was turned on its head in the 'In­side-out Model' (IoM) by Baum & Baum (2014), in which "clas­si­cal" en­do­cy­to­sis comes as the last evo­lu­tion­ary step, af­ter the internali­za­tion of the (fu­ture) mi­to­chon­drion:

Fig­ure 4. In­side-out model (IoM) for the evo­lu­tion of eu­karyotic cell or­ga­ni­za­tion. See text for de­tails. Source

A  Model show­ing the step­wise evo­lu­tion of eu­kary­otic cell or­ga­ni­za­tion from an eo­cyte an­cestor with a sin­gle bound­ing mem­brane and a gly­co­pro­tein rich cell wall (S‑layer) interac­ting with epibi­otic α‑proteobacteria (proto-mi­to­chon­dria).

B  We en­vi­sion the eo­cyte cell form­ing pro­tru­sions, aided by pro­tein-mem­brane in­ter­ac­tions at the pro­tru­sion neck. These pro­tru­sions fa­cil­i­tated ma­te­r­ial ex­change with proto-mi­to­­chon­dria.

C  Se­lec­tion for a greater area of con­tact be­tween the sym­bionts would have led to bleb en­large­ment and the even­tual loss of the S‑layer from the pro­tru­sions.

D  Blebs would have then been fur­ther sta­bi­lized by the de­vel­op­ment of a sym­met­ric nu­clear pore outer ring com­plex and through the es­tab­lish­ment of LINC com­plexes that, fol­low­ing the grad­ual loss of the S‑layer, phys­i­cally con­nected the orig­i­nal cell body (the nas­cent nu­clear com­part­ment) to the in­ner bleb mem­branes.

E  With the ex­pan­sion of blebs to en­close the proto-mi­to­chon­dria, a process that would have fa­cil­i­tated the ac­qui­si­tion of bac­te­r­ial lipid biosyn­the­sis ma­chin­ery by the host, the site of cell growth would have pro­gres­sively shifted to the cy­to­plasm, fa­cil­i­tated by the deve­lopment of reg­u­lated traf­fic through the nu­clear pore. At the same time, the spaces be­tween blebs would have en­abled the grad­ual mat­u­ra­tion of pro­teins se­creted into the en­vi­ron­ment via the peri­nuclear space through gly­co­sy­la­tion and pro­te­olytic cleav­age.

F  Fi­nally, bleb fu­sion would have con­nected cy­to­plas­mic com­part­ments and dri­ven the for­mation of an in­tact plasma mem­brane, per­haps through a process akin to phago­cy­to­sis whereby one bleb en­veloped the whole. This sim­ple topo­log­i­cal tran­si­tion would have iso­lated the en­do­plas­mic retic­u­lum from the out­side world, dri­ven the full de­vel­op­ment of a sys­tem of vesic­u­lar traf­fick­ing, and es­tab­lished strict ver­ti­cal trans­mis­sion of mi­to­chon­dria, lead­ing to a cell with mod­ern eu­kary­otic cell or­ga­ni­za­tion.

The E3 model pro­posed by Imachi, Nobu et al. (2020) is largely con­gru­ent with the IoM, but, in con­trast to the lat­ter, less de­tailed in the ex­pan­sion of the pro­tru­sions to fi­nally cover the fac­ul­ta­tively aer­o­bic organo­trophic part­ner (step c), and in the for­ma­tion of the pri­mor­dial nu­cleus by con­verting the pro­trusions into nu­clear pores (step d). Both mod­els re­main some­what vague as to when, in the se­quence of steps to­wards an in­ter­nalized proto-mi­to­chon­drion, a com­plete trans­for­ma­tion of the ar­chaeal genome into a eu­kar­y­otic genome might oc­cur. The genome of P. syn­trophicum MK‑D1 is or­ga­nized as a typ­i­cal pro­karyotic genome in a (cir­cu­lar) chro­mo­some. All known eu­kary­otic genomes are or­ga­nized in a vary­ing num­ber of (mostly) lin­ear chro­mo­somes. The im­por­tance of this tran­si­tion can be in­ferred from the fact that most genes en­cod­ing ribo­somal pro­teins are or­ga­nized as small and larger oper­onss in 'As­gard' ar­chaea, whereas in eu­kary­otes they are widely dis­trib­uted as sin­gle genes across sev­eral chro­mosomes.
 

Ad­den­dum You might en­joy read­ing in his own words how Masaru Nobu and his col­leagues went from be­ing sewage en­gi­neers to mi­cro­bi­ol­o­gists to evolu­tion­ary bi­ol­o­gists. Ad­dress­ing the reader, he ended his ac­count with: "...Every time you flush the toi­let, you may very well be feed­ing en­gi­neered re­ac­tor ecosys­tems that in­spired dis­cov­ery of the do­main Ar­chaea and cul­ti­va­tion of syn­trophic ar­chaea closely re­lated to our an­ces­tors".

In parts 3 +4 of Cul­ti­vat­ing the An­ces­tors…, I will show that Promet­hearchaeum syntro­phi­cum MK-D1 is not a mav­er­ick among the 'As­gard' ar­chaea, but a mem­ber of a fam­ily that oc­curs all over the world with sim­i­lar phys­i­o­log­i­cal and cel­lu­lar prop­er­ties, in­clud­ing de­pendence on syn­tro­phy, a pen­chant for bleb­bing, and those char­ac­ter­is­tic pro­tru­sions, the "tiny arms".