Two Tales of Sym­bio­sis

by Elio

I don't get tired of sym­bioses, some­thing I at­tribute to the Power Law of Sym­bio­sis I just made up: In­ter­act­ing genomes are more in­ter­est­ing than sin­gle ones by the n^th power of their num­bers, where n is a mat­ter of per­sonal pref­er­ence. Here I re­late two ex­am­ples that should make the point.

Im­muno­gold stain­ing of the ovary of the tick Ixodes rici­nus us­ing an­ti­bod­ies against the ma­jor fla­gel­lar pro­tein, FliD. Ar­rows in­di­cate the gold par­ti­cles present on the sur­face and in­side bac­te­ria-like struc­tures. Source

My first story is about a find­ing that should have caused its Ital­ian re­searchers to use a mild ex­ple­tive, such as "Corpo di Bacco!" ("By the body of Bac­chus!" I grew up in Italy, which en­ti­tles me to this bit of lin­guis­tic ir­rel­e­vancy.) What they found is amaz­ing. That a bac­te­r­ial en­dosym­biont had been found to dwell in­side the mi­to­chon­dria of ticks was sur­pris­ing in it­self (see a pre­vi­ous post), but to now find them to pos­sess what looks to be a com­plete set of fla­gel­lar genes, twenty-six in num­ber, is stun­ning. First, do these genes ac­tu­ally work, that is, ac­tu­ally pro­duce fla­gella? Con­vinc­ing proof of that is still lack­ing be­cause, as the au­thors point out, ob­serv­ing fla­gella in elec­tron mi­cro­scope sec­tions is not easy; they are very hard to dis­tin­guish when cut cross­wise. How­ever, these genes are tran­scribed and one of their prod­ucts can be iden­ti­fied on the sur­face of the en­dosym­bionts. In ad­di­tion, these genes have con­served do­mains and struc­tural fea­tures typ­i­cal of other fla­gel­lar genes.

A tick mi­to­chon­drion con­tain­ing three in­fect­ing bac­teria. Note that the mi­to­chon­drion is un­der­go­ing con­siderable dam­age. The empty por­tion of the mitochon­drion is en­cir­cled by the outer mem­brane only (ar­rows). b = bac­te­ria; m = ma­trix. Bar = 0.25 μm. Source

To put this in con­text, the sym­bionts, known as Can­di­da­tus Midichlo­ria mi­to­chon­drii are mem­bers of the rick­ettsiae, a group never be­fore shown to have fla­gella or fla­gel­lar genes. The Can­di­da­tus name is a tax­o­nomic straight­jacket de­not­ing that the or­gan­ism has not been cul­ti­vated on ar­ti­fi­cial me­dia (but, like many en­dosym­bionts, it may never well be!). So, do these un­usual rick­ettsiae use fla­gella for motil­ity? We would surely like to know.

This find­ing is not to­tally un­heard of among sym­bionts. En­dosym­bionts un­re­lated to these, such as those of aphids (Buch­n­era) and tse-tse flies (Wig­gleswor­thia) also pos­sess fla­gel­lar genes.  Keep in mind that in some bac­te­ria, fla­gel­lar com­po­nents are in­volved in se­cre­tory sys­tems, such as T3SS and T6SS. The au­thors posit:  It is rea­son­able to as­sume that in­tra­cel­lu­lar bac­te­ria such as Ca. M. mi­to­chon­drii and W. glossini­dia al­ter­nate trophic phases (in which fla­gella and motil­ity are not re­quired) with phases of the cy­cle in which a fla­gel­lar ap­pa­ra­tus is used for motil­ity or for other func­tions. But, as they point out, noth­ing is known about how Ca. M. mi­to­chon­drii en­ters the mi­to­chon­dria, there­fore it's not pos­si­ble to spec­u­late if fla­gella par­tic­i­pate in the in­va­sion of the or­ganelle, ap­peal­ing though this may be. Given the ex­tra­or­di­nary life habit of this bac­terium, we can ex­pect fur­ther de­vel­op­ments, some of which may turn out to be just as star­tling as these.

Let's fol­low the fla­gel­lar thread to a sec­ond story that un­cov­ered a role for fla­gella in a sym­bio­sis. Here a bac­terium and an ar­chaeon com­mu­ni­cate via the bacterium's fla­gella to es­tab­lish a syn­trophic (cross-feed­ing) re­la­tion­ship of mu­tual ben­e­fit. Both sym­bionts have long names, Pelo­tomac­u­lum ther­mo­pro­pi­onicum and Methan­oth­er­mobac­ter ther­mau­totroph­i­cus, re­spec­tively. The bac­terium fer­ments pro­pi­onate to ac­etate, bi­car­bon­ate, and H₂, a highly en­der­gonic or en­ergy un­fa­vor­able con­ver­sion. The re­ac­tion is dri­ven by the hy­dro­gen be­ing si­phoned off by the ar­chaeon for its methano­gen­e­sis. Pro­pi­onate  fer­men­ta­tion can pro­ceed as long as the par­tial pres­sure of H₂ is kept low by the ar­chaeon. Such in­ter­ac­tions have been known for some time. (See a most in­ter­est­ing re­view of such syn­trophic re­la­tion­ships by Win­ter­mute and Sil­ver.)

(A) P. ther­mo­pro­pi­onicum fla­gella ad­here to M. thermau­to­trophicus to fa­cil­i­tate be­tween-or­gan­ism H₂ ex­change. Source. (B) The FliD pro­tein at the tip of the P. ther­mopro­pionicum fla­gel­lum stim­u­lates methano­gen­e­sis by M. ther­mau­totroph­i­cus. Source.

What's new here is that when grown to­gether, these two strains form ag­gre­gates with the cells linked closely by the bacterium's fla­gel­lum. Now this is un­ex­pected. Per­haps there are other ex­am­ples, but I haven't heard of fla­gella be­ing used for some­thing other than lo­co­mo­tion, cer­tainly not for form­ing in­ter­species ag­gre­gates. The close prox­im­ity (about 2 μm) of the two part­ners is needed for ef­fi­cient trans­fer of the hy­dro­gen, which is the ap­par­ent rea­son why fla­gella are needed. The bond­ing of the bac­te­r­ial fla­gella is quite spe­cific, lim­ited to this ar­chaeon and only one other also known to form syn­trophic as­so­ci­a­tions with these bac­te­ria.

The two strains are high-tem­per­a­ture anaer­o­bic sewage di­gesters and can be grown singly in cul­ture, so this is not an oblig­a­tory part­ner­ship. But it's good for busi­ness, and not just as a me­chan­i­cal means of bring­ing the two part­ners close to one an­other. Tran­scrip­tome analy­sis of the ar­chaeon showed that a sub­stan­tial num­ber of genes in the ar­chaeon were up-reg­u­lated af­ter the con­tact with a pu­ri­fied pro­tein from the cap of the fla­gel­lum (FliD). The ad­di­tion of this pro­tein alone led to up­reg­u­la­tion of over fifty genes in­volved in the methano­gen­e­sis path­way and to in­creased methane for­ma­tion. These find­ings sug­gest that the bac­terium di­rectly com­mu­ni­cates with the ar­chaeon via its fla­gel­lum. This, too, is news, as in most in­ter­species sig­nal­ing is me­di­ated by small mol­e­cules and not by a struc­tural pro­tein.  One ex­am­ple of com­mu­ni­ca­tion via a pro­tein, which we posted be­fore, is seen in Pro­teus mirabilis, where a sur­face pro­tein en­ables cells of dif­fer­ent strains to rec­og­nize one an­other. Can we con­clude that the fla­gella of this bac­terium play two roles, one as the struc­ture used to keep the two part­ners of the con­sor­tium in prox­im­ity, the other as a sig­nal­ing mol­e­cule, telling the ar­chaeon that it's now time to make methane?

Such find­ings raise a lot of ques­tions. How wide­spread are syn­trophic in­ter­ac­tions be­tween species? What phys­i­o­log­i­cal phe­nom­ena, be­sides the meta­bolic, do they ad­dress? And, as Marx points out in an ex­cit­ing com­men­tary, con­sor­tia may serve as the as­sem­bled parts in syn­thetic bi­ol­ogy. For con­sid­er­a­tion of so­cial evo­lu­tion in mul­ti­species con­sor­tia, see an in­sight­ful col­lo­quium pa­per by Mitri et al. Mi­cro­bial con­sor­tia are be­ing found with in­creased fre­quency. Surely, this must af­fect our mind­set re­gard­ing mi­crobes in na­ture.

Ref­er­ence

Mari­conti M, Epis S, Sac­chi L, Big­giogera M, Sassera D, Genchi M, Al­berti E, Mon­tagna M, Bandi C, Baz­zoc­chi C (2012). A study on the pres­ence of fla­gella in the or­der Rick­ettsiales: the case of 'Can­di­da­tus Midichlo­ria mi­to­chon­drii'. Mi­cro­bi­ol­ogy (Read­ing, Eng­land), 158 (Pt 7), 1677−1683. PMID 22461487