Mystery Micrograph #22

[originally posted on 18.06.10 1:45am]
[EDIT 23.07.10: Btw, this mystery micrograph is still unsolved. Get crackin'. Ask questions if you need to.]

Apologies for the delay. To buy myself some time, I'll make it a really hard one this time. Like, a TEM. Bwahahaa. I'll give you a hint: these are not moth antennae.

Scalebars: 1um. To be referenced later.

Ultrastructure is particularly evil. Because it shows cells (cell slices) as they are, rather than how the researcher or artist thinks they are.

[25.06.10 HINT]: These structures are a synapomorphy/unique shared feature of one specific group of organisms.

Sunday Protist - Farming forams: a case of protistan agriculture

"WTF, it's Friday already!" Friday? What Friday? You saw nothing.

My previous two Sunday Protist attempts got derailed. With the first one, noticed there was quite a bit to say about them, and decided to postpone it for later as it was a big topic (and unrelated to my current work). Then I picked something relevant to my day job, y'know, two birds one stone, etc. And somehow that led me to paleontology. A warzone in paleontology. Complete and total clusterfuck. With potential inaccuracies here and there that I now need to sort out. Whilst we wait, I'll just do something quick: a case of a foraminiferan apparently growing bacteria and then eating them in perhaps one of the most non-human farming enterprises ever! (leafcutter ants are pretty much human at that phylogenetic distance...)

Textularia blocki lives on seagrass. Many forams have interesting associations with seaweeds, ranging from internal parasitism to epiphytic attachment, usually via secretions of sulfated mucopolysaccharides, a fairly common material in the extracellular matrix. T.blocki, however, is a freely motile foram. It leaves peculiar 'grazing traces' as it crawls along the seagrass, without damaging the tissue beneath it:

Left: T.blocki with grazing traces on blade of seagrass. Right: (Langer & Gehring 1993 J Foram Res)

As made evident in the diagram, the traces consist of two parallel 'walls', consisting of pale whitish adhesive material, presumably containing mucopolysaccharides, devoid of sand grains or other contaminants. Curiously, some forams carried sand grains along, without depositing them. These secretions are formed by pseudopodia, or the 'business' part of the foram: an intricate network of reticulated feet with amazing cytoskeletal properties. When these secretions are left alone in seawater for 48h, a lush garden of bacteria sprung up specifically along the secretion traces:

Bacterial gardens along the foraminiferan secretion traces. Note the relatively clean surface of the leaf outside the secretions, supporting that it is the adhesive mucous that attracts bacterial accumulation (Langer & Gehring 1993 J Foram Res)

When released back into the medium containing the seagrass lined with traces, the forams approach the nearest trace and follow along it, suggesting they use some form of chemical sensing to determine where the secretions are and how they are oriented. The speed is then reduced, suggesting the foram is then busy grazing on their bacterial harvest.

Thus, a 'mere' single celled organism can produce organised tracks of nutritious material, wait for their bacterial crop to grow, and subsequently harvest it. We like to think we invented agriculture. The more biologically-oriented among us point out leafcutter ant fungus gardens and aphid farming. Yet, agriculture has also evolved on the unicellular scale in a small humble foraminiferan living among blades of seagrass. Humbling, isn't it?

Interestingly, a similar behaviour has been described gastropods like slugs and limpets, as their mucous also attracts bacterial growth. Convergence: when a good thing is chanced upon multiple times, it will likely be kept by several lineages independently. This applies to language and cultural evolution as well as that of biological organisms.


We tend to have a deep conviction that cells are dumb blobs of goo, incapable of any sort of behaviour besides basic phototaxis or whatever. We think cells are just simple chemical response machines – which is true. But ultimately, so are we. There is no fundamental distinction between human social dynamics and the adventures of a crawling amoeba. The difference is all in the quantity and complexity of interactions – the higher the complexity, the more random (stochastic) the system appears (and to an extent, is). While I must concede that in terms of the number of components and pathways involved, human or ant behaviours are more complex than that of an amoeba, that does not mean the proverbial amoeba 'lacks' behaviour entirely.

I've mentioned the cellular behaviour stuff before, probably too often for regular readers. Apparently, that idea needs restating though. Also, as a cell biologist, I find it quite...well, pleasing. It's nice that, ultimately, my subjects are no more or less machine-like than humans or plants. Furthermore, where I was heading with this originally, I think part of our notion of cells being 'stupid' comes from the obsession with our own cells. Animal cells are, in fact, quite simple and developmentally retarded. The cause is cell specialisation driven by multicellularity. Eg. an epithelial cell can now afford to lose the ability to hunt around for prey, it no longer needs to coordinate movement in any sophisticated manner, the life cycle can be simplified to terminal differentiation.

Curiously, a similar problem plagues modern science and engineering: overspecialisation means that one must no longer have the same level of foundational education to survive, and thus we end up arguably knowing more about less, or perhaps knowing the same about less. I can suck at math or chemistry and get away with it. In the old days, people had to actually have a broader base just to function. Conversely, there was also less information floating around. Which is more efficient? Just as multicellularity vs. unicellularity, each system has its merits and drawbacks. So it's hard to tell.

A while back I found a paper on cellular complexity in multicellular vs. unicellular organisms that needs to be discussed in greater detail eventually...


---Random Link---
ChrisM over at the wonderful Echinoblog (about the cooler deuterostomes; ok, hemichordates and ascidians are cool too) wrote about sperm-eating ciliates infesting starfish.

Lots of things like sperm. For example, Monocystis is a gregarine with a penchant for earthworm sperm – infection rates are so high that if you slice up a worm from your backyard and smear the contents of its seminal vesicles on a slide, the chances are pretty good that you'll find some. And by 'some', I mean, LOTS. So if you're ever in the mood for some apicomplexans, all you need is an earthworm, a blade and a scope. There are parasites in pretty much anything and everything, so if you go around examining various animals, you may well find loads of cool protistan denizens in them. Many of which could be undescribed and, perhaps, new to science.

Reference
Langer, M., & Gehring, C. (1993). Bacteria farming; a possible feeding strategy of some smaller motile Foraminifera The Journal of Foraminiferal Research, 23 (1), 40-46 DOI: 10.2113/gsjfr.23.1.40

Carnivorous trees of the sea: Notodendrodes not as harmless as it looks

Remember Notodendrodes and the spicule tree? Don't they look so much like harmless trees sitting around sunbathing like their plant counterparts? Not all tree forams are harmless. The microscopic marine world is full of surprises, like trees waving around their long sticky network 'feet' to trap and devour any traveler that happens by. Here's some wonderful shots of Notodendrodes caught in the act:

The top left image shows a clump of Artemia caught by Notodendrodes, a big carnivorous tree foram. Note how the reticulopodia (pseudopodial networks) stretch between the branches like spiderwebs. Top right: SEM of the reticulopodial mesh of another species of Notodendrodes. Bottom: The tree foram in its natural setting, with a copepod attached (arrow). (Suhr et al. 2008 Mar Ecol Prog Ser)

There some nice foram videos on this YouTube page, including shots of reticulopodia and a fairly large foram moving about in situ. This movie by a Japanese researcher includes clips of Artemia being captured starting at 0:50.

Many forams are voracious predators, devouring anything from fellow protists to crustaceans and echinoderm and mollusc larvae. The following is Astrammina rara's rather impressive menu; all but two species were happily consumed:

However, not all forams are carnivorous. Some are mediocre at best at capturing prey, and some, like Crithionina, are quite bad. This suggests a range of feeding habits from detritovory to carnovory to omnivory. Note how Gromia (not a foram, despite looking vaguely similar; placement somewhat uncertain, though most likely either close to forams or a cercozoan) fails to capture any prey. Also, dead specimens failed to catch prey, indicating the capture is intentional and requires a fully functioning cell, and not an accidental adhesion to something sticky. In fact, there is evidence for specific targetting of certain prey, which wouldn't be much of a stretch as many forams are quite picky in choosing their test material.

I think this has some interesting – perhaps borderline philosophical – implications. Towards the end of the ciliate kleptoplasty post I mentioned how the traditional ecological terms often fail to describe the majority of life, which happens to be microscopic and play by some different rules. There's a greater problem in the approach of traditional ecology towards microbial life, however, and it even surfaced in a random chat with some ecology grad students. Namely, the treatment of all things microbial as the "bottom of the food web", ie. prey species created by evolution to feed cute fluffy animals. They have a similar attitude to plants as well: 'producers'. Fungi are 'decomposers'.

Probably to people tracking bird migration out in the field, such crude terms do just fine, and we all must make crude approximations somewhere (or drown in details). However, as in any simplification, there's always a danger of skimming over interesting outliers. I disagree with the blanket treatment of protists (and bacteria, and anything else) as the "bottom of the food web" for two reasons:

1. There are plenty of intricate interactions resulting in elaborate food webs (and, more generally, 'interaction webs'); a plethora of fascinating relationships is lost when one blurs them all into the 'prey for animals' category.

2. Feeding by animals forms but a very tiny part of the overall diversity of microbe-animal interactions. An ecological framework must account for symbionts (mutualists, parasites and commensals) along with predation. Toxoplasma, arguably the most successful parasite of vertebrates ever, is a wonderful example of 'lower trophic levels' leeching 'up' the food web and running the show. You can't really draw an arrow from a cat or human to the modest apicomplexan, as it doesn't really consume its slaves. But you can't really not draw that arrow. It's complicated.

(In fact, if organisms besides humans had Facebook, most of their relationship statuses would be set to "It's complicated". Groan all you want... =P)

Lastly, our forams mentioned above also have ecological consequences on the megafauna in their environments. Astrammina rara is benthic, meaning it lives on the ocean floor (or, technically, any substrate). Suhr et al (2008) mention past studies indicating lower-than-usual densities of marine fauna in particular areas; these areas seem to match up with Astrammina's distribution. Presumably, the effects of predation on small fauna and larvae can be seen on the larger scale.

Furthermore, the carnivorous forams seem to affect the survival strategies of the fauna around them (in hindsight, unsurprisingly): some echinoids have brood protection and settling strategies that may well have evolved in response to the lowly single celled protists they rightly fear. The authors suggest that the failure of Astrammina to capture larvae of the echinoid Acodontaster may be a result of the latter evolving a specific chemical defense against it.

The 'scum' from the bottom of the foodweb can come up to bite some 'higher' organisms in the ass – whodathunk?

Reference
Suhr, S., Alexander, S., Gooday, A., Pond, D., & Bowser, S. (2008). Trophic modes of large Antarctic Foraminifera: roles of carnivory, omnivory, and detritivory Marine Ecology Progress Series, 371, 155-164 DOI: 10.3354/meps07693

Sunday Protist - Giant tree of spicules: Spiculidendron

Christopher Taylor over at Catalogue of Organisms has a nice post on agglutinated Saccamminid foraminifera, and very recently wrote on the taxonomy and morphology of Pelosina, Pilulina and Technitella, wherein he brought up a fascinating paper on one hell of a bizarre foram: the 'spicule tree', initally mistaken for a gorgonian (sea fan). I'm going to leech off his find as he didn't specifically mention this tree foram in his post. Also, he mentioned Komokians before I did. Meanie. In all seriousness, go read his posts. For the phylogenetically inclined protistologists, the Komokian post is good food for thought.

I'm going to slack off a bit this time. For an overview of the huge clade of awesome that is Foraminifera, see my earlier post here; for another tree foram, see Notodendrodes here.

Foraminiferans are amazing creatures: some of them can be best described as giant cannibalistic carnivorous wads of sticky reticulated pseudopodia, capable of snaring and devouring small metazoans and Volvox colonies. They have the fastest microtubule growth rates in the eukaryotic kingdom - a whole two orders of magnitude greater than those of animals at a stunning 12µm/s! (animal cells grow microtubules at around 1-15µm/min.) (Bowser & Travis 2002 J Foram Res) Their pseudopodia are themselves capable of shearing flesh in a process so unique it deserved its own name: 'skyllocytosis' (Bowser 1985 J Protozool). Do not screw around with forams. They are scary.

Most of them also have shells, but that's a story for some other day. Well, many stories, for many days. Forams are a huge and diverse group.

The following specimen belongs to Astrorhizidae, a group of agglutinating forams - meaning their tests are composed of material from the environment, often very selectively picked. As implied by its name, the spicule tree, or Spiculidendron, composes its test entirely out of sponge spicules. Furthermore, this contraption reaches a stunning 60mm (6cm) in height, as a single-celled organism!

Plant, animal or protist? A foram tree to shame all foram trees. A giant spicule-covered monster from the Caribbean tropics. (Rützler & Richardson 1996 Biologie)

The paper mentions difficulties in determining whether the spicule tree bears a single nucleus or is coenocytic. Presumably, if it was that hard to find (though they had few specimens to work with), it may well be uninucleate like Notodendrodes. This would be quite cool as 6cm is one hell of a giant cell to be supported by a single nucleus. The cytoplasm also contains symbiotic dinoflagellates, making this tree foram even more like an actual tree.

Note that this strange monster of a foram was only described in 1996. The age of exploration is far from over.

References
Rützler, K., & Richardson, S. (1996). The Caribbean spicule tree: a sponge-imitating foraminifer (Astrorhizidae) Bulletin de l'Institut Royal des Sciences Naturelles de Belgique 66 (Suppl.), 143-151

Bowser, S. (2002). RETICULOPODIA: STRUCTURAL AND BEHAVIORAL BASIS FOR THE SUPRAGENERIC PLACEMENT OF GRANULORETICULOSAN PROTISTS The Journal of Foraminiferal Research, 32 (4), 440-447 DOI: 10.2113/0320440

BOWSER, S. (1985). Invasive Activity of Allogromia Pseudopodial Networks: Skyllocytosis of a Gelatin/Agar Gel The Journal of Eukaryotic Microbiology, 32 (1), 9-12 DOI: 10.1111/j.1550-7408.1985.tb03005.x

Conflict of Interest is not unique to corporate blogging

You may or may not be aware of the major kerfuffle on ScienceBlogs recently. If not, consider yourself lucky. Seriously, it's not that important. In a nutshell, SB launched a new blog on food science operated by someone in PepsiCo, SB readership exploded, SB withdrew blog, several very important bloggers left over it, and yeah. Basically, a scheme devised to remind me of how nice it is here on Field of Science, where we are truly independent, mostly blog about actual science (with apologies about this post) and have yet to see any drama *knock on wood* =D

Well, since all the big kids are doing it, I'll chime in too =P partly to procrastinate with take a break from writing about foraminiferan pseudopodia.

I don't really have a strong opinion on corporate blogging either way. It should be clearly labeled as such, just so we can estimate what the bias would be. On the other hand, it'd be nice to know what our brethren in the private sector are doing. They have labs and scientists and science over there too; one doesn't need a medieval institution for that. But again, there is a real potential of such a blog turning into a PR campaign. Which, actually, isn't too different from an independent blogger pushing a particular opinion or ideology. On the other hand, ScienceBlogs did fail public relations, and quite miserably too. From the looks of it, its bloggers weren't well informed. But still, that's a poor excuse to act like a cage full of rabid howler monkeys on caffeine tablets and low-grade acid.

I don't think automatically treating anyone with private funding as a 'corporate shill' and 'non-human immoral braindead moron' is a particularly wise or constructive thing to do. In other words, it's fucking moronic. Corporations are technically just a legal shell, and can't really write or do anything. They themselves don't have a physical presence. Corporations consist of people, who do have a physical presence, and are capable of writing and doing stuff. They're people like everyone else. Being employed does not suddenly make one a braindead zombie. In fact, can't the other side call academic bloggers "academic shills" and accuse them of merely parroting what the grant officers want to hear?

As all people, corporate employees have personal interests, desires, goals, demands and worldviews based on which they try to deal with all the former. These interests are not evil, nor is the 'pure' pursuit of science a saintly task. Sometimes – nay, often even – other people's interests conflict with our own. Who the fuck are we to judge our own interests and worldviews as 'morally superior' to anyone else's as if we, alone, have some god-ordained divine access to 'Higher Truth'? Sure, some views (hypotheses, if you will) stand up to facts (ultimately, sensory input) better than others. Which is why creationism is not on equal footing as evolution. At all. But one must remember that those people will act in ways that are founded on their beliefs and worldviews, as well as extrinsic restrictions. In other words, they're doing the best they can. Soulless* corporate 'shills' included.

*In the literal sense.

We all have conflicts of interest. Starting with the very basic fact that a lot of our blogs are known to friends, colleagues and *gasp* employers. I'm affiliated with a certain lab (and still sort of affiliated with another), I am funded by a specific university and have an employer. Obviously I'd have a conflict of interest whenever I write something potentially sensitive, like blogging about my department's research. That's little different from somebody in the private sector blogging about their industry with all the associated concerns. We all have political, social and financial interests to consider. (unless you're some isolated hermit in the middle of the tundra somewhere in Nunavut with a satellite connection)

Furthermore, people who actually do research (unlike those of us who just write about it, heh) generally need $$ for their activities. This $$, generally, needs to come from somewhere. Where do you think it originates? Siphoned off the Flying Spaghetti Monster's personal chequing account? Magically created in the lab of some mad scientist? If only. It comes from the evilest source of all: the bloody economy. Ok, perhaps you [wisely] stay the hell away from Big Science, and subsist entirely on federal grants. Where did you think that money came from? That's right: taxpayers. Ie, ultimately, the very private sector we all love to hate.

From the little I understand (still a long ways away from grantwriting), grants aren't exactly a no-strings-attached affair. You have to report your results eventually, having not only done something productive but also something very relevant to what you wrote in your grant application. I may be wrong, but that's the sense I'm getting. Please correct me if grants actually are free gifts of shiny money you can then spend on a giant fully-catered university-wide orgy with an open bar, on a boat cruise in the Seychelles. Not that federal grants can cover even a tenth of that...

If it's the former, then, presumably, your next step is to work towards securing the next grants. That is, your results should probably be of a kind that would encourage further funding in your field. Presumably, if you get funding for environmental topics, you'd be better off with results stating your Cute Fluffy Animal is on the brink of extinction rather than 'oh it's doing fine'. In that particular case, who the hell is going to dump more money into Cute Fluffy Animal research if it's not under some sort of threat? Conflict of interests much?


Even blogging about research papers is sensitive, especially within your own field. You have to balance opinion, factual accuracy and style without offending the authors. Some bloggers find it perfectly sensible to unleash a tirade against some paper they don't like, but I'd prefer not to sever potential relationships with people I've never met, even if I do think their paper is a piece of crap. Primarily for selfish reasons: at this point, I'm in no position to start collecting enemies in academia. Or anywhere, really.

If I were a truly independent blogger, that wouldn't fucking matter, and I'd probably make a point of devouring every crappy paper I come across for shits and giggles. Again, this isn't all too different from a corporate blogger generally speaking well of their employers and perhaps being more critical of their competition. Naturally, I'd be more inclined to publicly rip other labs' papers to shreds rather than my own.

This wasn't really about the ScienceBlog 'Pepsigate' incident much; drama fluff comes and goes. I think there's a bigger problem: too many people, including academics themselves, live in this magical bubble where conflict of interest and the bias it drives somehow fail to exist in the bastion of rational thought that is academia. Research, as soon as it's peer-reviewed, is automatically politically-neutral and scientifically-accurate. That sort of thinking is outright delusional, and dangerous. We are humans. And, like all humans, we are just trying to make ends meet in this distinctly unfriendly world, handicapped by the eons of accumulated evolutionary garbage and imperfections in our bodies, brains included. We are biased and selfish. We are also diverse and varied. And not a single one of us knows the 'Truth'.


I find it odd and annoying that neutrality/centrism tends to be universally politically unfavourable, sometimes absurdly so: people often think higher of their opposition than of anyone neutral. Neutrality is not necessarily symptomatic of indecision or indifference (although sometimes is, and for good reason), but rather often an admission of the intense complexity of the issue at hand. I think it's better to abstain from taking sides at all than make ill-informed ones based on oversimplified cases. For some reason, that view is surprisingly unpopular in some circles...

Anyway, I'll get back to actual science posting. Now you know why I rarely discuss controversial/political stuff here -- too complicated for my tiny little brain. Besides, protists are way cuter =D

New carnival in molecular biology and CoE#25

Sorry for the delays in posting - was out of town and away from internet, and then frantically scrambling to get back into the writing zone and get work done. Only half a month ago, another edition of the Carnival of Evolution went out: #25 at Culturing Science. Go check it out, she even has drawings for each heading!


Coming up soon is the first edition of the new MolBio Carnival, headed by Alejandro at MolBiol Research Highlights, where the first edition will happen (posts on the first Monday of each month). We need submissions (form here), and after a couple months, hosts. From the the carnival's main page:

We encourage the submission of posts discussing peer-review articles, techniques, books and related topics. Specific areas of interest include, but are not limited to: structure and function of proteins, nucleic acids and other macromolecules, gene expression and its regulation, signal transduction, apoptosis, developmental biology, cell cycle and cell growth, microbiology, biochemistry, structural biology, membrane dynamics and many others. Systems and synthetic biology-related posts are also welcomed.

So go on and share anything molecular biology related, which is perhaps the bulk of modern biology anyway ;-) (except my stuff -- really need to crank up the molecular details here someday...) Feel free to double or triple post or whatever to multiple carnivals. The more linkage action going on, the better.

Ok, the carnival's gonna be waaay better than my miserable failure at advertising it. So go hit that shiny submit button *sparkle*. And please help spread the word!


Finally, I find many old illustrations to be quite beautiful. This one is from 1938 (Myers, PNAS) discussing the sex life of forams:

Sunday Protist - Assorted oddballs

As I scramble to finish a chapter before my supervisor notices his hiring mistake, instead of writing out a mini-review paper about a single group of sorts, I'll use the opportunity to point out a few of the oddballs I've accumulated lately. Many of them have just a single paper, or a passing mention and a reference to a paper I can't get easily (and that would likely be in some language I can't read to begin with...), and thus they don't really make good weekly protists by themselves. But yet, many are too cool to ignore mentioning.

Our first exhibit is a peculiar association between a coccolithophorid haptophyte (small phytoplankton), Reticulofenestra sessilis, and a centric diatom, Thalassiosira sp.:

The thing in the centre is the centric diatom. The scaley things around are the coccoliths, or calcified scales, of the haptophytes Reticulofenestra clustering around it. The exact nature of this relationship is unknown, though presumably beneficial for the haptophyte, as R.sesslis is found almost exclusively attached to diatoms. Image by from nannotax.org; original citation - Gaarder & Hasle 1962 Nyü Mag Bot (which doesn't exist online *gasp*)

Speaking of haptophytes, here's another cool-looking one. There is quite a bit to say about haptophytes overall, just too lazy to do it right now. There is a post in the making though...

Umbellosphaera. The things on the surface are its coccoliths, of which each individual is intricately crafted into a chanterelle/trumped-like shape. SEM on the left from a nice image repository/course supplement by Isao Inouye from U Tsukuba, one of the Meccas of protistology. (Website is in Japanese, unfortunately for [most of?] us. I really need to learn Japanese someday...) Image of single coccolith on the right from eol.org.

Now for an obligatory ciliate. Trichodina is a cute little peritrich (group that includes the coiled-stemmed-trumpet Vorticella) that deserves more attention than just a pretty picture, but its looks can't wait to be exposed. Both the top and bottom sides have cilia, and the creature is like a miniature robotic vacuum cleaner, vacuuming the fish gills (or other substrates, like jellyfish) of bacteria and various other prey that accumulate there. In doing so, it causes fish disease, but the cute lil' thing didn't mean to!

Left: Trichodina 'vacuuming' fish gills (source). Middle: DIC image of the Trichodina 'sucker' (surprisingly from National Geographic, of all places). Right: Drawing of the ciliate. (HJ Clark 1866 Am J Sci) Will surely come back to it someday!

And last for today, this little critter is absolutely adorable. There's actually quite a bit to say about it, but I'm not gonna do it because some other blogger is far more qualified to write it up. Perhaps after the conference season calms down a little, said blogger could share their wonderful stories with us...

Apusomonas proboscidea. To paraphrase Opisthokont, 'cute Apusomonas' would be redundant. You see that little protrusion at the top? It wiggles 'spastically' as the critter crawls forward along its flagellum. If you're really keen check out the movies in this recent paper on apusomonads (TC-S alert!). Left: Karpov & Myl'nikov 1989 Zoologicheskiy Zhurnal (in Russ.) Right: Flemming Ekelund at ToLWeb (Apusomonas is really tiny...)

That's it for today. Am going out of town until middle of next week, will likely lack internet (eeek, how will I live?!), so if comments are mysteriously ignored, that's why.

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

Ciliate-in-a-test-tube

Who said test-tube babies were 'unnatural'?

Undella hyalina, a tintinnid ciliate. Tintinnids craft wonderful loricas out of organic materials, often studding them with bits of random gunk (but not in this case).
http://www.obs-vlfr.fr/gallery/album316/undellopsis_hyalina

There's something quite adorable about a ciliate who willingly crawls into a test-tube by itself. In fact, it actually makes its own test-tube. If only all the protists could just grown their own flasks, fill them with optimal media, and culture themselves*...

More to come soon!

*Technically, they do culture themselves, quite successfully too. Just not in conditions convenient for researchers...

Sunday Protist - Lagynion: bottled algae

Quick one today as I should really be writing a chapter, as well as the post on plastid thiefs some of you wanted. And haptophytes. Have I mentioned my ADD tendencies?

While I find ochrophytes (large group including diatoms and kelps) a bit too phycological for my tastes, some of them are actually really cool, especially Chrysophytes - the 'golden algae'. Chrysos include things like scaly flagellates (Paraphysomonas) and Dinobryon which makes colonies that look like trees of stacked wine glasses. A while ago we had bottled ciliates, and this time the Chrysophytes offer us a few bottled algae, especially the flask-shaped Lagynion.

A happy(?) clump of photosynthetic flasks, of Lagynion. Source: Micro*scope.

The lorica consists of organic material. The progeny following division are released as little zoospores bearing the ridiculously complicated flagella characteristic of ochrophytes (one of them too short to be easily visible). Then the zoospores settle down, become amoeboid and grow themselves a new flask. As far as I could gather, that's pretty much all there is to say about Lagynion at the moment. But it still looks pretty cool!

1. Side view. Arrowheads indicated a rib structure surrounding the 'flask'. 2 and 3: top views of three Lagynion cells showing optical sections through the base and the neck regions, respectively. 4. TEM of 'flask'. Note the plastids (C) and the nucleus (N). V - peripheral vesicles. In short, plastids in a bottle. (O'Kelly & Wujek 2001 Eur J Protistol)

In fact, there's a whole family of bottled, and often amoeboid, algae called Stylococcaceae (eg. see Nicholls 1987 J Phycol), but they are so obscure it's painful to find much literature on them, or even decent pictures. Especially since by the time they get digitised, a lot of the old images become completely illegible. But here's another member of the family bearing slightly different glassware, Chrysopyxis:

Source: Micro*scope

Now to do real work and then write up some of the really exciting stuff I came across lately. And crush my writer's block with something sharp and heavy. Really annoying when you can't write anything because, well, you can't write anything. Wish brains came with instruction manuals...

References
Nicholls, K. (1987). CHRYSOAMPHIPYXIS GEN. NOVA A NEW GENUS IN THE STYLOCOCCACEAE (CHRYSOPHYCEAE) Journal of Phycology, 23 (3), 499-501 DOI: 10.1111/j.1529-8817.1987.tb02537.x

O'Kelly, C., & Wujek, D. (2001). Cell structure and asexual reproduction in Lagynion delicatulum (Stylococcaceae, Chrysophyceae) European Journal of Phycology, 36 (1), 51-59 DOI: 10.1080/09670260110001735198

PS: Hardly relevant but kind of newsworthy: First Phaeophyte genome sequenced! (Cock et al. 2010 Nature) Until now, the only complete Stramenopile(=Heterokont) genomes were a couple diatoms and oomycetes. Ok, there's still many more to go but Phaeophytes can be interesting in terms of studying the evolution of multicellularity. Also, the ochrophyte clade is a phylogenetic mess; not that single whole genome data means much but could perhaps helps calm the harsh seas somewhat.