On The De­f­i­n­i­tion of Prokary­otes

by Nanne Nan­ninga

As will be ar­gued be­low the present de­f­i­n­i­tion of a prokary­ote is highly un­sat­is­fac­tory. To give an ex­am­ple: a prokary­ote is "a cell or or­gan­ism lack­ing a nu­cleus and other mem­brane-en­close or­ganelles, usu­ally hav­ing its DNA in a sin­gle cir­cu­lar mol­e­cule" (Brock, Bi­ol­ogy of Mi­croor­gan­isms, 10th Ed.). This  seems a sum­mary of the orig­i­nal de­f­i­n­i­tion of Stanier & van Niel (1962), which I quote for the sake of com­plete­ness: "The prin­ci­ple dis­tin­guish­ing fea­tures of the pro­cary­otic cell are: 1. ab­sence of in­ter­nal mem­branes which sep­a­rate the rest­ing nu­cleus from the cy­to­plasm, and iso­late the en­zy­matic ma­chin­ery of pho­to­syn­the­sis and of res­pi­ra­tion in spe­cific or­ganelles; 2. nu­clear di­vi­sion by fis­sion, not by mi­to­sis, a char­ac­ter pos­si­bly re­lated to the pres­ence of a sin­gle struc­ture which car­ries all the ge­netic in­for­ma­tion of the cell; and 3. the pres­ence of a cell wall which con­tains a spe­cific mu­copep­tide as its strength­en­ing el­e­ment". Today's per­cep­tion of these points amounts largely, as in­di­cated above, to the ab­sence of a nu­clear en­ve­lope in prokary­otes. It should be men­tioned that Stanier & van Niel in the above pa­per also wished to dif­fer­en­ti­ate a bac­terium from a virus and to in­cor­po­rate blue-green al­gae within the prokary­otic do­main.

Fig­ure 1. Elec­tron mi­cro­graph of DNA-ri­bo­some com­plexes. The ar­rows point to branches, pre­sum­ably re­flect­ing cRNA (mRNA). Mi­cro­drops from gra­di­ent frac­tions were placed on for­m­var cov­ered grids, fixed in for­ma­lin, ph 6.0, for 1–2 hr and pos­i­tively stained with 2% uranyl ac­etate, pH 5.0. Bar: 100 nm. Source

The pa­per of Stanier & van Niel ap­peared more than 50 years ago. In this con­tri­bu­tion I will at­tempt to present a more mod­ern de­f­i­n­i­tion of a prokary­ote, keep­ing in mind that one should dis­tin­guish be­tween two as­pects: its de­f­i­n­i­tion and its dis­tinc­tion from a eu­kary­ote. But, be­fore do­ing so I will in­sert an his­toric in­ter­mezzo.

In­ter­mezzo

Fig­ure 2. G. Stent's scheme of cou­pled tran­scrip­tion and trans­la­tion. Source

An al­ter­na­tive char­ac­ter­i­za­tion of prokary­otes al­ready emerged, though not ex­plic­itly, in 1964 through the study by Byrne et al. on the for­ma­tion of DNA-ri­bo­some com­plexes as an­a­lyzed by su­crose-gra­di­ent cen­trifu­ga­tion.  In those times su­crose gra­di­ent data were graph­i­cally ex­pressed with ra­dioac­tive counts on the ver­ti­cal axis and frac­tion num­ber on the hor­i­zon­tal axis. In the pa­per of Byrne et al. the fo­cus was on the cel­lu­lar or­ga­ni­za­tion of tran­scrip­tion and on the sta­bil­ity of RNAs, in par­tic­u­lar mRNA (then also named cRNA). Their la­bel­ing and frac­tion­a­tion ex­per­i­ments led to the fol­low­ing con­clu­sion: "Our re­sults sug­gest that some time af­ter the on­set of cRNA tran­scrip­tion on the sur­face of the gene, a ri­bo­some will at­tach to the RNA mol­e­cule. This event may sig­nal the be­gin­ning of polypep­tide syn­the­sis on the ri­bo­some. The ri­bo­some may then ad­vance along the cRNA strand fol­lowed by other ri­bo­somes, re­sult­ing in a con­tin­u­ous trans­la­tion of the ge­netic mes­sage into polypep­tide se­quences." And fur­ther on: "In a sense, ri­bo­somes in bac­te­r­ial sys­tems may be a rudi­men­tary form of the 'car­rier' ri­bonu­cle­o­pro­tein par­ti­cles be­lieved to trans­port cRNA from the nu­clei of higher or­gan­isms." An elec­tron mi­cro­graph of one of the frac­tions shows clus­ters of par­ti­cles with ri­bo­so­mal di­men­sions and threads, pre­sumed to be DNA and per­haps mRNA (Fig­ure 1).

Fig­ure 3. "Dis­persed strands of ge­nomic DNA with polysomes at­tached" of the hy­per-ther­mophilic ar­chaeon Ther­mo­coc­cus ko­dakaraen­sis vi­su­al­ized by the Miller tech­nique (1970). Bar: 200 nm. Source

Pro­tec­tion of nascent tran­scribed RNA was also a con­cern of G. S. Stent (1966): "What kind of sys­tem might as­sure in vivo re­moval of the nascent RNA from the tem­plate?" In the case of mRNA ri­bo­somes came to the fore and mRNA-pro­tec­tion be­came in­cor­po­rated into the frame­work of cou­pled tran­scrip­tion and trans­la­tion, that is trans­la­tion starts be­fore tran­scrip­tion has been fin­ished (Fig­ure 2). The con­cep­tual draw­ing of Stent be­came re­al­ity through the im­pres­sive elec­tron mi­cro­graphs of Miller et al. (1970). (See also: Pic­tures Con­sid­ered #1. Vi­su­al­iz­ing Cou­pled Tran­scrip­tion and Trans­la­tion in E. coli, by Elio, 2013).

Then, E. coli was still the model or­gan­ism. Some years ago cou­pled tran­scrip­tion and trans­la­tion has been vi­su­al­ized for the hy­per­ther­mophilic ar­chaeon Ther­mo­coc­cus ko­dakaraen­sis (Fig­ure 3) us­ing the Miller tech­nique (French et al. 2007). Thus, one can con­clude that in the bac­terium E. coli and in the ar­chaeon T. ko­dakaraensi cou­pled tran­scrip­tion and trans­la­tion are facts. Whether this ap­plies to all Ar­chaea re­mains to be seen. Be­cause eu­kary­otes lack cou­pled tran­scrip­tion and trans­la­tion, prokary­otes in this way, dis­tin­guish them­selves pos­i­tively (Mar­tin & Koonin, 2006).

The dis­tinc­tion be­tween prokary­otes and eu­kary­otes

Fig­ure 4. Struc­tural or­ga­ni­za­tion of the flow of infor­mation in pro- and eu­kary­otes. Source

As men­tioned above one should dif­fer­en­ti­ate be­tween de­f­i­n­i­tion and dis­tinc­tion. The fact that eu­kary­otes do not pos­sess cou­pled tran­scrip­tion and trans­la­tion — a neg­a­tive qual­i­fi­ca­tion for some, by the way — does not tell us much about eu­kary­otes. Also the ab­sence of a nu­clear en­ve­lope in prokary­otes — a neg­a­tive qual­i­fi­ca­tion too — is not very in­for­ma­tive. What is fun­da­men­tal in cells re­lates to the struc­tural or­ga­ni­za­tion of in­for­ma­tion pro­cess­ing, i.e. the flow of in­for­ma­tion from DNA through mRNA to pro­tein. Con­cep­tu­ally, this bears on the cen­tral dogma of mol­e­c­u­lar bi­ol­ogy. Thus, the main dis­tinc­tion be­tween pro- and eu­kary­otes lies in the pres­ence or ab­sence of cou­pled tran­scrip­tion and trans­la­tion, re­spec­tively (Fig­ure 4). Does this suf­fice as a de­f­i­n­i­tion for a prokary­ote? This ques­tion is eas­ier posed than an­swered. I may re­fer to an­other quo­ta­tion from Stanier & van Niel in the same pa­per men­tioned above: "The dif­fer­ence be­tween eu­cary­otic and pro­cary­otic cells are not ex­pressed in any gros fea­tures of cel­lu­lar func­tion; they re­side rather in dif­fer­ences with re­spect to the de­tailed or­ga­ni­za­tion of the cel­lu­lar ma­chin­ery" (ital­ics by Stanier & van Niel). The ab­sence of a cel­lu­lar struc­ture (a nu­clear en­ve­lope) can hardly be con­sid­ered an in­for­ma­tive state­ment when it is known that tran­scrip­tion and trans­la­tion are spa­tially cou­pled. The lat­ter re­flects the "de­tailed or­ga­ni­za­tion of the cel­lu­lar ma­chin­ery" and, I be­lieve, this should be part of a de­f­i­n­i­tion, as should mi­cro­scopic size and a cell wall.  If one con­trasts prokary­otic cy­to­plasm with that of a eu­kary­ote the pres­ence of mem­brane-bounded or­ganelles sus­pended in a dy­namic cy­toskele­tal frame­work ap­pears a dom­i­nant fea­ture in the lat­ter case. Such struc­tural dif­fer­en­ti­a­tion could hardly be ac­co­mo­dated for in a mi­cro­scopic cell. Also re­mem­ber that mi­to­chon­dria and chloro­plasts have prokary­otic di­men­sions. Fol­low­ing this rea­son­ing a prokary­ote can be con­sid­ered a walled cell of mi­cro­scopic size pos­sess­ing cou­pled tran­scrip­tion and trans­la­tion and a not-well dif­fer­en­ti­ated cy­to­plasm. Ac­cord­ing to our present knowl­edge this ap­plies to Bac­te­ria and Ar­chaea. Struc­turally there is a "deep gulf" (Lane, 2011) be­tween prokary­otes and eu­kary­otes. To what ex­tent this bears on their phy­lo­ge­netic re­la­tion­ships re­mains to be seen.

Two ob­ser­va­tions seem at vari­ance with the fore­go­ing. Firstly, there is the re­mark­able mem­brane com­part­men­ta­tion of a planc­to­mycete bac­terium like Gem­mata ob­scuriglobus (see here in STC). How­ever, three-di­men­sional re­con­struc­tions sug­gest that the vi­sual com­part­ments are due to a sec­tioned lobed con­for­ma­tion of an E. coli-rem­i­ni­cent or­gan­ism (Santarella-Mell­wig et al. 2013). Im­pli­cat­ing a prokary­otic or­ga­ni­za­tion. Sec­ondly, nu­clei do not seem to be de­void of pro­tein syn­the­sis, though the na­ture of the pro­teins in­volved are not known (David et al. 2012). Pre­sum­ably, an ex­cep­tion that might prove the rule.

 

Ref­er­ences

  • Brock Bi­ol­ogy of Mi­croor­gan­isms (2003). 10th Ed., by Madi­gan MT, Mar­tinko JM & Parker J. Pear­son Ed­u­ca­tion, Inc., Up­per Sad­dle River, NJ 07458, USA
  • Byrne R, Levin JG, Bladen HL & Niren­berg MW (1964). The in vitro for­ma­tion of a DNA-ri­bo­some com­plex.  Proc Natl Acad Sci USA, 52, 140−148 PMID 14192650
  • David, A, Dolan BP,  Hick­man HD, Knowl­ton JJ, Clavarino G, Pierre P, Ben­nink JR, & Yewdell JW (2012). Nu­clear trans­la­tion vi­su­al­ized by ri­bo­some-bound nascent chain puromy­cy­la­tion. J. Cell Biol, 197, 45−57 PMID 22472439
  • French SL, San­tan­gelo TJ, Beyer AL & Reeve JN (2007). Tran­scrip­tion and trans­la­tion are cou­pled in Ar­chaea. Mol Biol Evol, 24, 893−895 PMID 17237472
  • Lane N (2011). En­er­get­ics and ge­net­ics across the prokary­ote-eu­kary­ote di­vide. Biol Di­rect, 6, 35 PMID 21714941
  • Mar­tin W & Koonin EV (2006). A pos­i­tive de­f­i­n­i­tion of prokary­otes. Na­ture, 442, 868 PMID 16929275
  • Miller OL Jr, Hamkalo BA & Thomas CA Jr (1970). Vi­su­al­iza­tion of bac­te­r­ial genes in ac­tion. Sci­ence, 169, 392−395 PMID 4915822
  • Santarella-Mell­wig R, Prug­naller S, Roos N, Mat­taj IW, & De­vos DP (2013). Three-di­men­sional re­con­struc­tion of bac­te­ria with a com­plex en­domem­brane sys­tem. PloS Biol, 11 (5), e1001565 PMID 23700385
  • Stanier RY & van Niel CB (1962). The con­cept of a bac­terium. Arch Mikro­biol, 42, 17−26 PMID 13916221
  • Stent GS (1966). Ge­netic tran­scrip­tion. Proc R Soc Lond B Biol Sci, 164, 181−197 PMID 4379509

 

Nanne Nanninga

Nanne Nan­ninga is Emer­i­tus Pro­fes­sor of Mol­e­c­u­lar Cy­tol­ogy at the Uni­ver­sity of Am­s­ter­dam Swammer­dam In­sti­tute for Life Sci­ences

 

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