by Merry and Elio
Organelles were endosymbionts that either made good or were enslaved, depending on your point of view. Either way, some of their genes now reside in the nuclear genome of their eukaryote host. We also know that there are some bacterial endosymbionts living today within multicellular eukaryotes. Can their genes also make such a jump to their host genome? And if so, what then?
The first evidence for such a transfer was reported in 2002. The participating endosymbiont was Wolbachia pipientis. Wolbachia are among the most avid professional endosymbionts, found in more than 20% of all known insect species (and in other groups as well, such as nematodes.) They're notorious for their blatantly sexist tactics. Since they are maternally inherited – like organelles – their preferred habitat is the cytoplasm of female reproductive tissues of their insect hosts. From there, they manipulate host reproductive biology to insure their own survival, basically by favoring in several ways the population of infected females. That location also gives them a leg up for lateral gene transfer (LGT) to the germ line of their host. Furthermore, although their genome is highly streamlined, it still contains a surprising number of mobile DNA elements (that is, insertion sequences and retrotransposons) that might increase their chances for LGT.
In that first report, a Wolbachia genomic fragment was found in the X chromosome of its insect host, the adzuki bean beetle (Callosobruchus chinensis). Later work demonstrated that 360 Wolbachia genes – about 30% of the genome – had been transferred to the beetle's nucleus. A second instance was reported in 2006, this time involving a Wolbachia endosymbiont of a nematode, the human-parasite Onchocerca volvulus. These nematode endosymbionts also reside in the reproductive tissues of their hosts where they are essential for host reproduction. (See our earlier post about the role of this Wolbachia pathogen in river blindness.)
Last year, another research group chimed in with their findings of Wolbachia genes in fruit flies, wasps, and nematodes. In the tropical fruit fly, Drosophila ananassae, virtually the entire Wolbachia genome had been transferred. Using PCR, they demonstrated that 44 of 45 Wolbachia test genes were present in the fly DNA. With fluorescence in situ hybridization (FISH) using probes for two Wolbachia genes, they located the insert on the fly's autosomal 2L chromosome. Breeding experiments confirmed that the insert was inherited as a well-mannered Mendelian autosomal trait, not maternally as are the endosymbionts.
It is one thing for a genome fragment from an endosymbiont to be incorporated into the nuclear genome of its host, quite another for it to be transcribed, translated, and used by that host. What is the fate of those hundreds of transferred genes? Few were found to be transcribed in either the adzuki bean beetle or the tropical fruit fly. In the beetle, most had been degraded to pseudogenes, but low levels of transcription were detected for a few. In the fly, about 2% of the 1206 transferred genes are transcribed. The 5' end of the transcript from one of those genes has a 5' mRNA cap – an important step in the maturation of mRNA in eukaryotes. But there wasn't much of that transcript made, perhaps a million times less than for the actin gene. The odds are small, the hurdles high. Still, at this point, the possibility that transcripts of some of those genes function in some host tissues cannot be ruled out. (For a recent review of the role of LGT in eukaryote evolution, click here.)
So, what's going on? Why are so many genes transferred, with so little obvious purpose? Are the Wolbachia squirreling away their genes for safekeeping, or is there some other reason for their massive transfer to the host's nucleus? A mystery. Whether they function in their new location or not, these transferred genes serve to remind us yet once again that genes are mobile, genomes dynamic. Given the huge numbers of cells and organisms, even very low probability events can – and do – happen, creating new evolutionary possibilities.
The D. ananassae researchers argue that although the reported transfers so far are few, they are not to be dismissed as mere novelties. We quote:
"Because W. pipientis is among the most abundant intracellular bacteria and its hosts are among the most abundant animal phyla, the view that prokaryote-to-eukaryote transfers are uncommon and unimportant needs to be reevaluated."
Ah, the rough wooing of macrosymbiont and microsymbiont. And who can say which entity is "running the show"?
It's like those "Chinese box" souvenirs: boxes inside boxes inside boxes. Or Russian nesting dolls.
This is a post I will be discussing in class on Wednesday, Elio and Merry. Much kudos and tips of metaphorical hats.
1. We all suffer from from what I tell the students to call "colicentricity"---what we easily observe in one system is assumed to be the rule throughout nature. We microbiologists know better. So the large scale transfer of DNA may be MUCH more common (and perhaps ongoing) than we suppose:
Gladyshev, EA, Meselson M, and IR Arkhipova. (2008). "Massive horizontal gene transfer in bdelloid rotifers." Science 320: 1210 - 1213.
Who knew that rotifers could be "sponges" for diverse genetic information (and how wonderful that Matt Meselson was part of this--what a career!)? It could be called something like "omnisexuality" (and I will avoid the obvious puns). More seriously, I have wondered about other organisms that undergo cryptobiosis, like tardigrades: do they do this kind of thing as well?
2. Regarding Wolbachia---what is with the bacteriophages?
Bordenstein SR, et al. (2006). "The tripartite associations between bacteriophage, Wolbachia, and arthropods." PLoS Pathol. 2(5): e43.
Does this mean that phages infest the cytoplasm of insect cells inhabited by Wolbachia, and even move from cell to cell and insect to insect in search of new Wolbachia, or is there some niche outside the insect where the bacterium grows and is susceptible to phage attack? We know that the association is old, yet the phages seem intact (I would expect them to be sandblasted down to pseudogenes by the dead hand of Darwin if they were not currently infectious to their host).
This takes me back to my old friend Caedibacter and its symbiosis with Paramecium (and the remarkable "killer" trait). This too may be due to the co-opting of a lysogenic phage!
Jeblick J and J Kusch. (2005). "Sequence, transcription activity, and evolutionary origin of the R-body coding plasmid pKAP298 from the intracellular parasitic bacterium Caedibacter taeniospiralis." J. Mol. Evol. 60: 164 - 173.
So we have to think of ourselves as not simply a series of ecological niches for our microbiota to inhabit and with which to interact. It seems as if our cells themselves contain a series of microenvironments in which prokaryotes can grow...and their own DNA elements (phages, transposable elements) are all jockeying for position at the same time.
It's a wonderful if dizzying time to think about microbiology.
Posted by: Mark O. Martin | November 10, 2008 at 11:24 AM