The Bac­terium That Doesn't Know How To Tie Its Own Shoelaces

by Elio

A greater mi­cro­bial won­der­land there isn't than the one in­side cells of in­sects. Many, per­haps most, in­sects har­bor bac­te­r­ial en­dosym­bionts that are full of phys­i­o­log­i­cal, ge­nomic, and struc­tural sur­prises. To con­firm our pre­dilection for the sub­ject, go to Search on the right of this page and en­ter "en­dosym­bionts." Or read re­cent re­views (click here or here).

A hack­berry peti­ole gall psyl­lid just af­ter emerg­ing from the gall on a hack­berry. The leaf is yel­low be­cause it is au­tumn. The in­sect is only 3 to 4 mm long. Credit: Nan­cy Moran, Univ. of Ari­zona. Source

In many cases, bac­te­r­ial en­dosym­bionts are known to pro­vide their host with needed nu­tri­ents, in oth­ers their role re­mains un­known. The clas­sic ex­am­ple is Buch­n­era, the en­dosym­biont of aphids. Aphids feed on plant sap, which is rich in sug­ars but poor in needed amino acids. The bac­terium pro­vides them, and thus is es­sen­tial to its host. Mat­ters can get com­pli­cated, as when two en­dosym­bionts part­ner to syn­the­size tryp­to­phan, one mak­ing an early pre­cur­sor in the biosyn­thetic path­way, the other tak­ing it the rest of the way. Part­ner­ships of this sort (ac­tu­ally, mé­nages á trois) seem not to be un­usual. This too we dis­cussed ear­lier. Other bac­te­r­ial en­dosym­bionts, no­tably Wol­bachia, ma­nip­u­late the sex life of their in­sect hosts for their own ad­van­tage. Thus, the world of bac­te­r­ial en­dosym­bionts of in­sects has turned out to be ever more var­ied and strange.

En­ter Car­sonella rud­dii, or, if you're a purist, 'Can­di­da­tus C. rud­dii' (be­cause it hasn't been culti­vated out­side its host – nor is it ever likely to be).

It has the puni­est of genomes among en­ti­ties that could be called bac­te­ria. With a measly 160 kb or so of DNA, en­cod­ing some 182 pro­teins, it is the small­est "bac­te­r­ial" genome pub­lished to date (but we've heard that even smaller ones are soon to be re­ported). The host of Car­sonella is a psyl­lid, in par­tic­u­lar the hack­berry peti­ole gall psyl­lid. Psyl­lids are also known as the "jump­ing plant lice."

A psyl­lid bac­te­ri­o­cyte with tubu­lar Car­son­ella sur­rounding the nu­cleus. DNA is stained with DAPI. Source

Is such a tiny ge­nomic en­dow­ment suf­fi­cient to sus­tain life? Among the miss­ing genes are some might­ily es­sen­­tial-sound­ing ones, for ex­am­ple, some needed for mak­ing ri­bo­somes, for DNA repli­ca­tion, and for mem­brane func­tions. Can such a crea­ture re­ally be called a bacte­rium? Is Car­sonella on the way to be­com­ing an or­ganelle? If so, what good is it to the host? Genes re­quired for mak­ing sev­eral of the amino acids needed by the host (e.g., his­ti­dine, pheny­lala­nine, and tryp­to­phan) are ab­sent or non­func­tional. On the other hand, if it doesn't pay for its up­keep in some man­ner, how come host cells are loaded with so many car­sonel­las?

It's true that the Car­sonella genome is ex­tra­or­di­nar­ily stream­lined, ergo ef­fi­cient. For in­stance, 90% of its ORFs over­lap in at least one di­rec­tion. Ninety-two per­cent of them are tan­dem out-of-frame over­laps on the same strand. Car­sonella ORFs are close to 20% shorter than those of other in­tra­cel­lu­lar in­sect endo­sym­bionts. But, ef­fi­cient or not, the Car­sonella genome is smaller than that of some mi­to­chon­dria and chloro­plasts, both of which re­quire the prod­ucts of many genes that they pre­vi­ously trans­ferred to the host's nu­cleus. Is this the case here? We don't know yet be­cause no hosts of Car­sonella have been com­pletely se­quenced. So, how does Car­sonella get by with what is left in its genome? It hardly seems to be large enough to sus­tain life as we know it.

What are the other pos­si­bil­i­ties? Rather than get­ting re­quired gene prod­ucts from Car­sonella genes in the nu­cleus, could some in­stead be pro­vided (by a kind of prokary­otic em­pa­thy) by "nu­clear" mi­to­chon­dr­ial genes? Such pro­teins would have to be tar­geted to both the mi­to­chon­dria and the sym­bionts. An­other pos­si­bil­ity is that there could be an­other bac­te­r­ial en­dosym­biont lurk­ing some­where, but as yet none have been found. Or, as seems even more un­likely, could our cat­a­log of re­quired genes be in part er­ro­neous, with the genes present in Car­sonella ac­tu­ally be­ing suf­fi­cient for life?

We have some in­for­ma­tion about gene trans­fer from en­dosym­bionts to Buch­n­era-car­ry­ing aphids. How­ever, the mean­ing of this is murky be­cause these genes are de­rived from α‑proteo­bac­teria, whereas the Buch­n­era are γ‑proteobacteria.

Trans­mis­sion elec­tron mi­cro­graph of a psyl­lid bac­ter­iocyte. A, bac­te­ri­o­cyte; B, en­dosym­biont; C, un­identified elec­tron-dense ag­gre­gate. Bar, 2 μm. Source

Car­sonella presents fur­ther enig­mas on the cel­lu­lar level. Its cells are ex­tremely long tubules, many tens of μm in length and around 5 μm in width. They don't look like re­gular prokary­otes in EM sec­tions be­cause, among other things, there is no sign of a nu­cleoid. (Is their DNA con­tent so small as to es­cape vi­su­al­iza­tion?) They look like nearly uni­form bags of ri­bo­somes, ex­cept for some mys­terious elec­tron-dense in­clu­sions. In fact, the crea­tures don't look like any­thing, bac­te­r­ial or oth­er­wise, that we can re­call. Let's ex­pect that fur­ther at­ten­tion will be paid to the struc­ture and mor­phol­ogy of these un­usual crea­tures.

If these ques­tions were not enough, let us add one more: Are such en­dosym­bionts des­tined for fur­ther re­duc­tion, pos­si­bly with cat­a­strophic con­se­quences to them­selves and, who knows, maybe even their hosts?

Here's a ques­tion for the as­tute among you (all our read­ers are as­tute by de­f­i­n­i­tion): What would it take to an­swer all those ear­lier ques­tions? Which ‑omics would you go for first? More ge­nomics of hosts, pro­teomics of the sym­biont, tran­scrip­tomics of both? If we were grant-grant­ing agen­cies, we'd be hard put to know which to fund first.