Criminally photosynthetic: Myrionecta, Dinophysis and stolen plastids

The microbial world is full of vicious beasts. Yes, much of microbial life is cute and cuddly in one way or another. But that doesn't stop many of them from making wolverines seem docile by comparison. There is an entire mafia out there built around...organ theft; including some multicellular players as well, in case you thought animals were saintly. Today we'll look at some famous thieving masterminds of the plastid black market, but keep in mind that there are many more fascinating relationships involving keeping entire organisms or their parts alive within the host, and vastly more oddities that have still escaped human attention (not hard to do, actually).

Let's start off the messy subject with a pretty diagram summarising the major plastid hoarding events of the [moderately] distant past:

Pac-Man!* Today all we need to do is appreciate the overall big picture: there were numerous symbiotic events and by about tertiary endosymbiosis, it gets messy. Not pictured are the cases of more-or-less transient kleptoplasty (plastid-theft), which would do serious harm to the readability and aesthetic qualities of this diagram. (Keeling 2004 Am J Bot; free access) For those keen on extra gory details of plastid endosymbiosis, see this recent review.
*If somebody were to make a game of Pac-Man: Endosymbiosis Edition...

Today's plastidial saga will involve an arduous journey from the cyanobacterium to the red algal endosymbiont of the cryptomonad, to the subsequent ingestion by a ciliate and a dinoflagellate. In fact, just keep in mind that the cryptomonad itself is the result of a hungry heterotroph getting a habit of devouring red algae and developing a case of terminal indigestion, ultimately gaining a plastid and plastid-targetting genes in its own nucleus. The cryptomonad in particular happens to be really awesome in another way: it actually still retains the original, eukaryotic, red algal nucleus of its former prey! That nucleus has been badly shrunk in the wash, and the genome is essentially on crack, but that's a long story for some other day.

Just so you get an idea of what a cryptomonad roughly looks like:

Cryptomonas. Note its very diminutive size. Source: Micro*scope.

We're about to move on to the sleazy thieving ciliates and dinoflagellates. But first, we must establish how kleptoplasty (lit. plastid theft) differs from endosymbiosis. To clarify, I use 'symbiosis' as a general term for an intimate interaction between two different species, including parasitism, mutualism and commensalism. Thus, an endosymbiont needn't feel the same way about the relationship as its host, and very often doesn't. Keep in mind that it is often not very obvious which exact category the symbiosis falls into, as nature doesn't particularly care for our naming fetish.

Endosymbiosis, in the context of organelles and other intracellular stuff, typically entails the complete engulfment of another organism by the cell. Once gene transfer occurs between the genomes of the two organisms, some declare the endosymbiont is now officially an organelle. The endosymbiont-organelle debate is old, stale and utterly pointless; thus, as I have declared in a previous post, I like to call plastids and mitochondria 'endosymbionts' and the more questionable cases, like Perkinsela, 'organelles'. That way, I can piss off just about everyone. Ha!

Then there is the much-awaited plastid theft, where only the plastid itself of the failed endosymbiont is retained, with the rest of it typically digested away. The katablepharid Hatena which Labrat wrote a wonderful post about (as well as Merry at Small Things Considered), is a striking case of kleptoplasty (and only discovered this past decade!). The intensity of kleptoplasty, as well as endosymbiosis, vary greatly from transient plastids (or endosymbionts) that are not essential to the host, to mostly permanent plastids or endosymbionts that are retained indefinitely, capable of reproducing on their own, and completely obligatory for the host's survival. This is nicely summarised in this diagram from a recent review on acquired photosynthesis by Stoeker et al 2009:

Two ways to get a plastid: 1) steal a plastid-bearing alga and lock it in your basement keep it alive within you (endosymbiosis); 2) mug the alga, steal its plastid and try to keep it alive yourself. Along the two paths lie multitudes of intermediate steps different in the persistence of the plastid (how long it lasts) and how dependent the host is upon it. (Stoecker et al. 2009 Aquat Microbiol Ecol)

In the endosymbiotic pathway, nucleomorphs (and the original plastidial prokaryotic genome) suggest the permanent associations we know among the 'normal' algae come from the endosymbiotic path, as there is evidence for whole host retention at some point. However, the data do not entirely rule out some independent secondary plastid acquisition via kleptoplasty rather than endosymbiosis. As for tertiary plastidial symbionts, it gets fun. The classic persistent cases like Kryptoperidinium tend to have a whole endosymbiont, nucleus and all, so the endosymbiotic pathway is also more likely, cut things like Dinophysis, on the other hand, are just weird.

Now, at last, our long-awaited thief: the ciliate Myrionecta rubra (=Mesodinium rubrum):

Myrionecta rubra (originally Mesodinium rubrum); c - cirri; ChC - chloroplast complexes; ECB - equatorial ciliary band (Taylor et al. 1969 Nature) Right: SEM of Myrionecta by Takayama Haruyoshi (more awesome micrographs here)

As you can see, this ciliate bears plastids - a rather non-ciliate activity. In fact, if you slice it up, you'll find that the plastids are very carefully arranged at the periphery:

N - cryptomonad nucleus; M - ciliate macronucleus (note the difference in chromatin organisation); note how the plastids are not only predominantly on the cell periphery but also tend to all face outward! (Oakley & Taylor 1978 Biosyst)

The ciliate captures a cryptophyte, takes its plastids -- along with the nucleomorphs, pyrenoids and other plastid-associated stuff, as well as cryptomonad mitochondria -- and packages them up in their own little compartments. Furthermore, the nucleus is also retained and consistently packaged in an entirely separate package from the plastids. Quite remarkably, the cryptomonad nucleus remains transcriptionally active! (Apparently, Elio beat me to it in 2007. Grrr) Presumably, maintaining an active host nucleus would help keep the plastids functional longer.

Oddly enough, I have difficulties finding anything on the exact process of crypto acquisition - I initially thought it just phagocytoses them, but a friend of mine studying weird plastid aquisition thinks they may actually employ myzocytosis - sucking out the contents of its prey through a 'straw', like many other alveolates do: this may explain the segregation and separate enveloping of the plastid and crypto nucleus. This would require Myrianecta to be quite fast and well-coordinated; the speed is there as it tends to jump instead of moving gradually (details here).


There is a plot twist to this story. A stroke of irony, or poetic justice, or karma if you're into such things. The thieving ciliate itself gets mugged...by a dinoflagellate!

At first glance, Dinophysis caudata is a normal photosynthetic dino, which isn't particularly surprising as roughly half of them are (most with their own plastids). Dinophyceans are quite trippy morphologically, which made it even more frustrating that Dinophysis appeared impossible to culture, despite being photosynthetic. For a while, no one could figure out what exactly was wrong with it. Turns out, its plastids aren't its own, and are rather cryptomonad-like. Great, so it kleptoplasties the cryptos, let's just grow it in a jar full of them! Again, no luck - for some reason, Dinophysis appeared incapable of ingesting the cryptomonads!

It was all rather perplexing until someone figured out the problem in the 2000's, publishing the first successful culturing attempt in 2006 (Park et al. 2006 Aquat Microbiol Ecol). Here's what was missing:

Dinophysis (the jug-like thing with a conspicuous flagellum) sucking the plastids out of Myrionecta, who's rolled up into a small, whimpering ball by this point. (Park et al. 2006 Aquat Microbiol Ecol)

Not only is Dinophysis caudata a stinkin' thief, but it can't even do the primary stealing itself - the dino requires Myrionecta to do all the dirty work of packaging up the plastids. But it gets messier. First, a summary of the plastid's plight:

Dinophysis ingests plastids from the ciliate Myrionecta, who in turn stole them from a cryptomonad. Who, if you recall, obtained it a long time ago as a red algal endosymbiont. Who, of course, obtained the original plastid as a cyanobacterial symbiont. I think it ends there though. That poor cyanobacterial genome has been through a lot! (Wisecaver & Hackett 2010 BMC Genomics)

Now, whether Dinophysis also bears proper plastids of its own is up to heated debate at the moment. It looks like I'm not the only one thoroughly confused by it, and sorting out this issues is slightly beyond the responsibilities of a mere blogger at the moment, so let's leave this part of the story explicitly vague. It seems like Dinophysis may somehow supplement its own stock with the stolen plastids, as it appears to have plastid-targetting genes in its own genome (Wisecaver & Hackett 2010 BMC Genomics). However, there are also cases of Dinophysis carrying plastids that appeared very non-cryptomonad, and most likely to be of dinoflagellate origin (Garcia-Cuetos et al. 2009 Harmful Algae).

The chaos is quite understandable: it is actually very difficult to determine the nature of a relationship between two organisms, especially on the microscopic scale, and especially when one is inside another. It's often hard to distinguish a permanent from a transient relationship, and a mutualistic from a parasitic one. While there is strong direct evidence that the dino sucks plastids out of Myrionecta, that does not necessarily mean all of its plastids originated there. Or that it lacks its own (though that would make sense). Or more importantly, that the various research teams are even looking at the same bloody organism! Speaking of which, Myrionecta and Dinophysis appear to be in a 'bit' of taxonomic mess too, so I'll just let the professionals fight it out amongst themselves.

While that's going on, one cannot help but wonder how many such 'unconventional' relationships there really are. Food webs are not as direct as people think, the once one peers a little further than the usual stereotyped interactions (predator, parasite, prey, producer, whatever), ecology actually becomes an interesting (admittedly, fascinating!) subject. On that note, I think we should really be careful when trying to force terrestrial and macroscopic ecological terms onto the microbial world -- and by careful, I think we should perhaps come up with a system specialised for microbial life from the very beginning. While we seldom see one animal rip out an organ of another and keep it alive for itself, organelle theft is actually not all that uncommon. Life on the cellular level is weird to us, and many traditional terms simply fail to describe it.

There's a whole black market of utterly bizarre microbial interactions out there. We are only scratching the surface.

References
Garcia-Cuetos, L., Moestrup, �., Hansen, P., & Daugbjerg, N. (2010). The toxic dinoflagellate Dinophysis acuminata harbors permanent chloroplasts of cryptomonad origin, not kleptochloroplasts Harmful Algae, 9 (1), 25-38 DOI: 10.1016/j.hal.2009.07.002

Johnson, M. (2010). The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles Photosynthesis Research DOI: 10.1007/s11120-010-9546-8

Johnson, M., Oldach, D., Delwiche, C., & Stoecker, D. (2007). Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra Nature, 445 (7126), 426-428 DOI: 10.1038/nature05496

Keeling, P. (2004). Diversity and evolutionary history of plastids and their hosts American Journal of Botany, 91 (10), 1481-1493 DOI: 10.3732/ajb.91.10.1481

OAKLEY, B., & TAYLOR, F. (1978). Evidence for a new type of endosymbiotic organization in a population of the ciliate Mesodinium rubrum from British Columbia Biosystems, 10 (4), 361-369 DOI: 10.1016/0303-2647(78)90019-9

Park, M., Kim, S., Kim, H., Myung, G., Kang, Y., & Yih, W. (2006). First successful culture of the marine dinoflagellate Dinophysis acuminata Aquatic Microbial Ecology, 45, 101-106 DOI: 10.3354/ame045101

Stoecker, D., Johnson, M., deVargas, C., & Not, F. (2009). Acquired phototrophy in aquatic protists Aquatic Microbial Ecology, 57, 279-310 DOI: 10.3354/ame01340

TAYLOR, F., BLACKBOURN, D., & BLACKBOURN, J. (1969). Ultrastructure of the Chloroplasts and Associated Structures within the Marine Ciliate Mesodinium rubrum (Lohmann) Nature, 224 (5221), 819-821 DOI: 10.1038/224819a0

Wisecaver, J., & Hackett, J. (2010). Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata BMC Genomics, 11 (1) DOI: 10.1186/1471-2164-11-366