The Ancestry of the Malarial Plasmid Revealed

ResearchBlogging.orgSuppose you’re nearing the end of your life. In a strange twist of fate, you won the lottery. You decide to split the jackpot equally between your two children. While one child uses the money to fund a charity dedicated to fighting poverty, the other one uses it to start the crime syndicate he has always been dreaming of! Such might be the tale of the evolution of the malaria parasite, where an algal plastid stars as the unlikely jackpot.

Both apicomplexa and dinoflagellates inherited a red algal plastid from their forebears. Most dinoflagellates use this plastid for photosynthesis, trapping energy from the sun. Apixomplexans took a shadier path with this plastid when some of them became infectious parasites, like the malaria parasite that kills millions of people every year. They use this plasmid, the apicoplast, not for photosynthesis, but to synthesize fatty acids and other metabolites that are necessary for these parasites to enter host cells. From a human perspective, the apicomplexa are definitely the black sheep in the Alveolate family tree (below).

The malaria parasite, plasmodium falciparum, infecting red blood cells (source National Geographic).

The genes that lie on the plasmids in dinoflagellates and ampicomplexans reflect their different lifestyles. The dinoflagellates’ plastid only contains ‘photosynthetic’ genes and not much else. The apicoplast has genes that are involved in several different metabolic pathways, such as fatty acid and heme biosynthesis. The overlap between the two plastid genomes is virtually zero, making it difficult for scientists to compare them and come to meaningful conclusions about their ancestry.

Complicating matters, some closer parasitic nephews of the apixomplexa (like Cryptosporidium) have no plastid at all! This either means that the apicomplexan and dinoflagellate ancestor acquired an algal plastid independently from each other OR that photosynthesis / the entire plastid had been lost several times in different lineages. Using the lottery analogy, the question boils down to whether apicomplexans and dinoflagellates both won the lottery, or whether their common ancestor was the lucky winner, passing on its spoils to its common descendants? Since evidence was so sparse, both hypotheses garnered support in the scientific community.

Since protist family relationships can get complicated pretty quickly: a phylogenetic tree of apicomplexa, dinoflagellates and Chromera Velia.

Luckily a new player looking to break the stalemate entered the field recently: Chromera velia. This little bug turns out to be a closer photosynthetic relative of apicomplexa than the dinoflagellates are, and thus has the potential to settle some difficult ancestry issues. A team of scientists from Czechia and Canada sequenced the entire plasmid of C. velia to find out where exactly the malarial plasmid came from.

As you can see in the Venn diagram below, both the plastids of C. Velia and a related algal species (imaginatively known as CCMP3155) contain all the genes that are present on the apixomplexan and dinoflagellate plastid. On their turn, all these genes can be found back on the plastid found in red algae. The simplest way to explain this pattern is to say that all these plastids derived from a single red algal ancestor. It thus seems that the ancestor of apicomplexa and dinoflagellates got lucky in the lottery, and obtained this plastid by endosymbiosis after which the lineages diverged.

Cool venn diagram of the plastid gene contents of various protists. The apicomplexan and dinoflagellate plastids share almost no genes at all. Since both C. Velia and CCMP3155 have a slightly bigger entire gene repertoire, the plastids of apicomplexa and dinoflagellates seem to have lost different genes during their evolution. The boxed genes have never been seen in green algea.

From a plastid’s perspective, evolving from a photosynthetic C. velia-like organism into an organism with a parasitic lifestyle seems to have mainly been accompanied by gene loss. The authors provide evidence that many plastid genes had already migrated to the nucleus in the ancestor of dinoflagellates and apicomplexans, but that it continued after the lineages diverged. Perhaps some of these losses and migrations were exaptations for the different walks of life these protists would come to develop.

Many of the protists in this branch of the tree of life, including C. velia, live in symbiotic relationships with coral reefs. Could it be that the apicomplexans started their parasitic lifestyle by infecting coral cells with which they lived in close contact? I find this prospect both fascinating and terrifying. Fascinating because this research started with a desire to know where the malaria parasite came from, and in this quest for knowledge learnt more about its ancestry and evolution in general than we could have hoped. It is also terrifying because we are trying to eradicate a parasite that seems to have been infecting different forms of life on earth for nearly half a billion years.

Is malaria the price we now pay for a symbiotic relationship that existed hundreds of millions years before the first humans opened their eyes for the first time?

Janouskovec, J., Horak, A., Obornik, M., Lukes, J., & Keeling, P. (2010). A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1003335107

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8 comments to The Ancestry of the Malarial Plasmid Revealed

  • Dunbar

    How’s this for undead scary things:
    A. Fokine, P.G. Leiman, M.M. Shneider, B. Ahvazi, K.M. Boeshans and A.C. Steven et al., Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry, Proc. Natl Acad. Sci. USA 102 (2005), pp. 7163–7168.

  • Since when did you convert to protist blogging? =D

    Without having yet read the cited paper (but having heard about its research at great lengths before ;-) ), some quick points off the top of my head:

    - photosynthetic organisms also use plastids for non-PS related activities like fatty acid synthesis (there’s this whole convoluted pathway in plants we had to learn about; some plants use a mixture of eukaryotic and prokaryotic pathways with plenty of transport back and forth across the plastid membrane!); the plastid in apicomplexa has just lost its PS ability; presumably, the non-PS related pathways have also been modified somehow – I’ll need to read/ask about that…

    - apicomplexans are far from being the sole parasites among alveolates; there are heaps of parasitic and endocommensal/endomutualist ciliates and dinos as well; curiously, the phylogenetic fog near the divergence of apis and dinos may suggest a parasitic/endosymbiotic ancestor for dinos, rather than apis being the ones gone rogue (eg. Leander & Keeling 2003 TrEE).

    It is quite suspicious that many of the early-branching dinos are either parasites or symbionts (eg. perkinsus – parasite; oxyrrhis – heterotroph (non-PS); Symbiodinium et al – PS symbionts of corals, etc). Similarly with Chromera et al. and Colpodellids (parasites) – which IIRC branch on the api side – the dino+api ancestry seems parasitic at that point. The glaring omission of data around the ciliate divergence in the tree doesn’t help the situation much either. Caveat: this may have changed in the last year…quite difficult to keep up with eukaryotic phylogeny sometimes!

    - overall, the common plastid origin between dinos and apis has been more or less settled a while ago. The bigger question that still plagues the field is whether the vast supergroup encompassing Alveolates+Stramenopiles/”Heterokonts”+Rhizaria+Hacrobians shares a common red algal plastid origin – the Chromalveolate Hypothesis. Again, it is rather awkward that the early-diverging lineages (forming a bit of a “ladder” on the respective trees rather than their own clade) tend to be not only non-photosynthetic but also rather silent about their plastid-owning heritage. The senior author of the PNAS paper is a rather strong proponent of the Chromalv Hyp as there are some gene fusions (eg. discussed in Keeling 2009 JEM) and other molecular data supporting this group. Others are a bit more skeptical (eg. Bodyl et al. 2009 TrEE). Either way, once this gets sorted out (hopefully it will eventually…), there will probably be much learned about the mechanisms of evolution, speciation trends, etc.

    Ok, I really do have a chapter to write, for work… AFAIK, said chapter had nothing to do with spamming blogs w loooong comments >_>

  • And PS: The diversity of apis is simply breathtaking. While Plasmodium and Toxo steal all the attention, there’s an amazing variety of other apicomplexans out there, infecting pretty much anything that moves. Or could once contemplate moving. Gregarines are particularly awesome: look ‘em up on scholar and be amazed! In fact, here’s a pretty cool page about them:

    It has been estimated somewhere that roughly-speaking, there should be at least one species of apicomplexan specialised for each species of arthropod – a group some very erroneously claim to be the largest in terms of diversity. (that claim is so utterly absurd it makes me laugh…) Also, some of these apis are themselves [hyper]parasitised by microsporidia, and, of course, bacteria!

    Ok, I’ll try to shut up now, srsly…

  • Since when did you convert to protist blogging? =D

    It must be because of your shining protist blogging example ;).

    Thanks again for your insightful comment!

    The potential link between parasitism, commensalism and symbiosis in this clade is really fascinating. Just the thought that an ancient symbiotic (?) relationship between a protist and invertebrate, spawned this whole range of parasites and symbionts is breathtaking. The dinos/apis really carved a succesful niche for themselves over millions of years..

    Thanks for the links to the papers, those should be enough keep be busy tonight ;)! The Chromalveolate hypothesis was mentioned in this paper, but I left it out to keep the story flowing and simple. As more plasmids get sequenced, I’m sure this issue should be sorted out. As a complete outsider, I have a feeling that endosymbiosis is such a rare event, that you must come with pretty convincing arguments if you want to say a similar endosymbiotic event took place in a monophyletic lineage. Time will tell I gues

  • After a random chat today, it’s not yet outdated that ancestral dinos were actually…parasitic/endosymbiotic! So it seems like the free-living dinos ‘redeemed’ themselves from their parasitic origins, rather than apis being the ones ‘gone rogue’.

    Endosymbiosis is actually not that rare; there’s plenty of cases ranging from curious to absofuckinglutely surreal that just sadly never get mentioned anywhere outside the field… of course, losses are still more likely than gains. But not always. Often excess structures can be ratcheted onto a system via aforementioned constructive neutral evolution — the host can lose critical pathways, for example, and become [nearly] eternally dependent upon the endosymbiont. Shining example: mitochondria. And plastids (the metabolic pathways therein rather than just photosynthesis).

    Now, whether dino/api ancestors really were coral-dwelling – I doubt anyone has much of an idea. The question is being looked into though *glances at stacks of coral-derived cultures in the corner* ;-) But just another case of parasitism/endosymbiosis being, rather counterintuitively, reversible. Not much, but enough to occasionally yield us a ‘clean’ ‘free-living’ creature from a sea of ‘criminal’ parasites*!

    * I tend to like parasites and not consider them evil at all, and even slightly dislike the notion: we proud “free living” creatures are just as dependent on other life forms as parasites. Just less intimate.

    Before I forget: nice [though slightly aging] review of plastid symbiosis with a really awesome diagram, Keeling 2004 Am J Bot

    Good thing protist blogging does not lie neglected while my own blog gets overgrown with weeds =D. I’m gonna try and finally post something tonight…

  • The most awesome thing about blogging about Protists is that Psi comes over and posts amazingly interesting comments about everything containing lots of great information :)

    It might be scary, but the presence of plastids in malaria could also be quite a useful tool in terms of combating the disease. Because malaria are eukaryotic parasites they don’t have a huge number of targets that differ from human cells, but one very clear difference that does exist is the plastid and the plastic genome.

    Endosymbiosis is only rare when you’re not looking at algae. Within the algae it seems to be quite a common occurrence (I covered it a little here: and arguments over monophylogeny/polyphylogeny can get very, very involved.

    • Now, whether dino/api ancestors really were coral-dwelling – I doubt anyone has much of an idea. The question is being looked into though *glances at stacks of coral-derived cultures in the corner* But just another case of parasitism/endosymbiosis being, rather counterintuitively, reversible. Not much, but enough to occasionally yield us a ‘clean’ ‘free-living’ creature from a sea of ‘criminal’ parasites*!

      Parasitic/endosymbiotic dino-ancestors and redeemed parasites? Wow, that’s a really cool hypothesis that would make an amazing story.. I know I’ll be keeping out a close out for papers on this issue! I have difficulty placing Chromera in this scenario though.. Since it branches of within the apis, wouldn’t this require a second ‘redemption’ independent of the other dinos if we assume the dino+api ancestor was parasitic?

      The most awesome thing about blogging about Protists is that Psi comes over and posts amazingly interesting comments about everything containing lots of great information

      I have to agree with you 100% on this one! The lure works every single time ;) (j/k of course)!

  • Actually, don’t know if it was mentioned in the paper or not, Chromera seems to be in very close association w corals, if not an endosymbiont like the more famous dinoflagellate Symbiodinium. Thus, it would actually make a lot of sense that Chromera retained photosynthesis while its ancestors (and presumably, those of both dinos and apis) already became closely associated with other organisms (eg. endosymbiosis). The transitional stage where the ancestors where presumably photosynthetic (at least up until the divergence of Chromera) but already endosymbiotic/parasitic, is indeed quite perplexing.

    I can get more info on this next week if you’d like. They all went away on a retreat I wasn’t invited to due to being a lowly undergrad, grrr =(

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