We've all heard of the primary endosymbiosis of bacteria that eventually became mitochondria* and plastids, on two separate occasions (three if you count Paulinella plastid origin). Some have heard of secondary, and maybe even tertiary, plastid endosymbiosis (eg. brown algae with red algal plastids). There's a fascinating case of tertiary endosymbiosis where an entire diatom inhabiting a dino (Kryptoperidinium), etc. Another interesting phenomenon is the endosymbiosis resulting in other essential 'organelles', eg. Polynucleobacter in Euplotes(Görtiz 2006 in Prokaryotes 1:364-402). While plastids have been transferred about the tree several times, secondary endosymbiosis of mitochondria or whole non-photosynthetic eukaryotes seems to be extremely rare. Thus, the following case of an endosymbiosis of a kinetoplastid by an amoeba I find to be rather interesting.
*Well, there's still remnants of a crackpot adherence to the autogenous model of mitochondrial origin...
Meet Perkinsela (formerly Perkinsiella; Dyková et al. 2008b), an endosymbiont of amoebae that took until Hollande 1980 to be recognised as an organism rather than organelle! (although Grell 1973 Protozoology (p.363) does suggest a link to the endosymbiosis theory that was just becoming established at that time). Here's the amoebozoan host Neoparamoeba with an arrow pointing to Perkinsela:
(Eva Dyková, Tolweb Perkinsiella page)
This endosymbiont's life cycle has become completely confined within the host cell, as it is perpetrated along with nuclei upon host cell division. It is often found in a strange 'bipolar' form, with nuclei opposite of each other across the massive mitochondrion (which contains the kinetoplast - a dense disk of mitochondrial DNA unique to Kinetoplastids, which include Trypanosomes, the cause of African Sleeping Sickness), and in close association with the host nucleus:
(Dyková et al. 2003 Eur J Protistol; 8 shows Neoparamoeba with its endosymbiont (NN - host nucleus, K - kinetoplast (mitochondrial DNA), n - Perkinsela nucleus; 9 - Perkinsela itself. Note the two nuclei across the kinetoplast from each other (c- cytoplasm))
The nature of this endosymbiotic relationship remains unknown, although it seems to be mutualistic as the host and the endosymbiont both die without each other (Dyková et al. 2008b).
The endosymbiont is a sister group to Ichthyobodo, and even contains the splice leader sequences characteristic of Euglenozoa (the larger containing group of kinetoplastids, diplonemids and euglenids (remember Euglena?)) (Dyková et al. 2003; 2008b). Here's a tree to orient yourselves: (because everyone knows what Jakobids and Diplonemids are...feel free to go here for the bigger picture ^.^)
(Simpson et al. 2006 Trends Parasitol.; family tree of creatures with 'hockey puck' mitochondrial DNA...the intelligent designer was definitely tripping out on some serious stuff when he made this clade ^.^)
(Let's just say Neoparamoeba is an Amoebozoan. I have no desire to sort out Amoebozoan taxonomy at this hour, as it's a fucking mess. I have three trees before me from various periods, and the burning urge to rip all my hair out is a little too much. Seriously, Amoebozoa are just fucked up, as morphology-based classification failed more abysmally than usual there. It's hard to determine morphological features of something so...amoeboid ^^. I challenge a certain taxonomist who reads this to blog about their phylogeny! Have fun =P)
Interstingly, both Neoparamoeba and Ichthyobodo are fish gill parasites. While Neoparamoeba is an opportunistic parasite (Young et al. 2007) (ie it can also live freely; a more vicious example of opportunistic parasitism is Naegleria, which is harmless until it accidentally gets into a brain - it happens to love neural tissue!), Ichthyobodo is an obligatory ectoparasite. ('ectoparasite' means it attaches to the surface of the host cell to drain it of its 'juices', instead of going completely inside).
Fish gills seem to be rather fertile ground for parasites of all levels of devotion; for the chances of passing by one when you live in water are pretty good. It seems like the long-term close association between Neoparamoeba and Ichthyobodo parasitising off the same host has led to this intimate endosymbiosis - would be interesting to know the approximate timescale of the divergence between Perkinsela and Ichthyobodo, to see how long it can take for such relationships to evolve.
Here's the Neoparamoeba opportunist in action:
(Lovy et al. 2007 Vet Pathol; A - amoeba, E - fish epithelial layer; bar = 3um)
To summarise what I'm talking about:
(M - mitochondrion with kinetoplast; N - nucleus; HN - host (Neoparamoeba) nucleus)
If we were to analyse the Perkinsela genome, it would likely show signs of substantial genome reduction, due to it being no longer necessary to keep the entire set (depending how old the relationship is, of course). What would be even more exciting is if gene transfer to the host nucleus has already occurred! Perhaps the mitochondrion-targetting genes may go first; as far as I know, whether host-to-endosymbiont-nucleus targetting genes exist is still poorly understood. There are cases of host-to-endosymbiont-plastid targetting (dinoflagellates Karenia, Karlodinium...), however; and endosymbiont mitochondria tend to disappear rather early in endosymbiosis, so it's surprising to find it so prominent here.
Which makes one wonder...perhaps the host is keeping the endosymbiont for its mitochondrion? The cytoplasm is extremely reduced, so that the cell appears to be little more besides a nucleus or two and a kinetoplast. Could the kinetoplastid mitochondrion be capable of something the Amoebozoan one is not, that also happened to be useful for the amoeba? Doesn't seem very likely, but who knows... perhaps the ancestral Perkinsela was engulfed by the predatory Neoparamoeba as prey, and led to the mitochondrial analogue to kleptoplasty ('stealing of plastids' from prey practised by some predatory protists; sometimes they'll keep photosynthetic (algal) cells around for their plastids until they die - could be how cyanobacterial endosymbiosis first started)?
Or is Perkinsela just a really good parasite, successful to the point of no longer needing to even try, enjoying its free ride along with the host? This doesn't explain why Neoparamoeba dies without it, though. I guess all it would take is for the host to lose a gene or two essential for producing something that is made and exported by the endosymbiont/parasite; thereby fixing a dependency upon it. But I'm just rambling at this point...
There seems to be no mention of basal bodies/centrioles in Perkinsela ultrastructure studies; this worries me. kDNA replication is molecular cell biology on potent hyperhallucinogenic acid, and is a susbtantial topic best left for another day. In Trypanosomes, the final steps of kinetoplast replications require a system of fibrils attached to the flagellar root; the mitochondrion is tightly associated with the basal bodies (Liu et al. 2005 Trends Parasitol). If Perkinsela evolved from a 'stuck' amastigote kinetoplastid (ie. one in a non-flagellar stage of its life cycle, although that doesn't seem to happen in modern Ichthyobodo...), it could still retain a pair of centrioles, devoid of flagella. However, those should be fairly visible in EM.
I'm have this nagging feeling that I'm not making much sense anymore... >_> To wrap this up, there's also potential endosymbiotic association between the amoebozoan Thecamoeba and a labyrinthulid species. The labys seem to be able to proliferate at will without destroying the host, thereby seeming rather non-parasitic at the moment (Dyková et al. 2008a) Interesting...
Microbial diversity is amazing as is, but as soon as you start treating a cell as a potential ecosystem in its own right, the hidden universe of intracellular parasites and symbionts is overwhelming. This is where those popular charts showing the majority of biodiversity as invertebrates are just abusrd - each and every one of them is a possible ecosystem for microbial life, both bacterial and eukaryotic, and each and every cell thereof is yet another niche. And every protist is a possible ecosystem for some other protists, or prokaryote. Sometimes, those relationships persist and develop, and, on occasion, blur the line between organism and organelle.
So I wonder: is Perkinsela now an 'organelle'?
(This is why you should support basic biological research in addition to biomed; one cannot tackle cancer before understanding how single cells work in the first place. The 'higher' biology lies in the fundamentals, not select, limited cases like humans or mice...)
DYKOVA, I. (2003). -like endosymbionts of spp., relatives of the kinetoplastid European Journal of Protistology, 39 (1), 37-52 DOI: 10.1078/0932-4739-00901
DYKOVA, I., FIALA, I., DVORAKOVA, H., & PECKOVA, H. (2008). Living together: The marine amoeba Thecamoeba hilla Schaeffer, 1926 and its endosymbiont Labyrinthula sp. European Journal of Protistology, 44 (4), 308-316 DOI: 10.1016/j.ejop.2008.04.001
DYKOVA, I., FIALA, I., & PECKOVA, H. (2008). Neoparamoeba spp. and their eukaryotic endosymbionts similar to Perkinsela amoebae (Hollande, 1980): Coevolution demonstrated by SSU rRNA gene phylogenies European Journal of Protistology, 44 (4), 269-277 DOI: 10.1016/j.ejop.2008.01.004
Liu, B., Liu, Y., Motyka, S., Agbo, E., & Englund, P. (2005). Fellowship of the rings: the replication of kinetoplast DNA Trends in Parasitology, 21 (8), 363-369 DOI: 10.1016/j.pt.2005.06.008
Lovy J, Becker JA, Speare DJ, Wadowska DW, Wright GM, & Powell MD (2007). Ultrastructural examination of the host cellular response in the gills of Atlantic salmon, Salmo salar, with amoebic gill disease. Veterinary pathology, 44 (5), 663-71 PMID: 17846238
SIMPSON, A., STEVENS, J., & LUKES, J. (2006). The evolution and diversity of kinetoplastid flagellates Trends in Parasitology, 22 (4), 168-174 DOI: 10.1016/j.pt.2006.02.006
YOUNG, N., CROSBIE, P., ADAMS, M., NOWAK, B., & MORRISON, R. (2007). Neoparamoeba perurans n. sp., an agent of amoebic gill disease of Atlantic salmon (Salmo salar)☆ International Journal for Parasitology, 37 (13), 1469-1481 DOI: 10.1016/j.ijpara.2007.04.018