Sunday Protist – Scary nematode-eating forams and their amazing feet of doom

Poor, poor nematodes...

In the interests of public safety, I must reiterate once again what should be so painfully apparent from the last few posts on forams: If you ever find yourself shrunk to a milimetre or less, DO NOT fuck with forams. Ever.

It's a fairly known fact around these parts that [unicellular] forams can devour [multicellular] animals. But thus far we've just had giant tree forams like Notodendrodes show us the terrifying force of microbial nature. Notodendrodes is notably bigger than its prey, so the embarrassed metazoa have an excuse there. As for giant planktonic forams – well, those eat things only slightly larger than themselves, you may say. In which case you must be almost insatiable. But, as usual, there's more: rather small, unassuming Ammonia tepida devouring nematodes, copepods and gastropods unarguably larger than itself.

Like other forams, Ammonia uses its amazing reticulopodia (lit. "net-feet") to trap and entangle prey. Then, it penetrates its prey's exoskeleton or cuticle and forcefully rips apart the insides to shreds, bringing back phagocytosed chunks towards the main cell body for digestion. This process is creepy enough to warrant its own term: skyllocytosis (Bowser 1985 J Prootozool). All that's left behind is an empty cuticle with a hole. By the way, the prey are devoured within 24 hours. And apparently forams are pretty much always hungry. Imagine being violated by masses of dynamic and powerful net-like pseudopodia and torn to pieces from the inside. Doesn't sound fun. Feels good to be big, doesn't it?

Ammonia tepida vs. nematodes. c and d show before and after shots of one such encounter. Sometimes a second foram joins for a threesome. (Dupuy et al. 2010 J Foram Res)

As for copepods...the following sentence from the paper raises some concern: "Despite vigorous attempts to escape, copepods could not free themselves from the pseudopodial mesh."(Dupuy et al. 2010 J Foram Res) Most of us have seen copepods one time or another. For the world of their scale, they're quite strong. And yet they cannot escape. Neither can snails, whose shells are all that remains after a few hours. Have I mentioned foram reticulopodia are simply amazing?

Ammonia tepida vs. copepod (a) and juvenile snails (b,c). Note how the copepod is partially eaten already towards the right. d,e - SEM view of the ventral (umbilical) end of the foram. Little bumps (pustules) are thought to potentially act as 'teeth' and used to grind tests and cuticles. Some other forams are thought to do this with diatoms as well. (Dupuy et al. 2010 J Foram Res)

You may wonder how foram pseudopodia get to be so special. They possess many unique properties, many of which have yet to be understood. One of the more striking features is the rate of microtubule growth. While microtubules of animal cells grow at about 1-15µm/min, microtubule assembly in some forams can reach a stunning 12µm per second (Bowser & Travis 2002 J Foram Res). They manage this by possessing a unique third conformation of tubulin: helical filaments (in addition to the usual protofilaments/'tubes and free dimers).

Transformation of tubulin between helical filaments and free dimers appears to require no ATP, and thus would progress quite rapidly. Furthermore, tubulin of helical filaments can transform directly to the tubules, much faster than regular polymerisation from free dimers. The idea is that tubulin is stored in helical form (crystalised, if you will), and then transported to the site of active growth, and used for a quick and efficient supply of the growing 'tubes with fresh tubulin (Welnhofer & Travis 1996 Cell Motil Cytosk). Thus, it is perhaps not overly surprising that foraminiferan tubulins are highly diverged, suggesting selective pressure for the foram-specific modifications (Habura et al. 2005 MBE). This is yet another example of bizarre alterations by a protist of typically conservative aspects of eukaryotic biology.

SEMs of foram pseudopodia entrapping prey; in this case, Artemia. (Bowser et al. 1992 J Protozool)

To have an idea of what the microtubule cytoskeleton looks like in action, here's a stolen video of plant epidermis cortical microtubules marked with AtEB1:GFP:

In vivo timelapse of cortical microtubules marked with (+)-end binding GFP growing in a tobacco leaf epidermis. Picked this one because it has a scalebar (10µm) and a timestamp (in seconds; movie is sped up, but the whole thing lasts a minute); I do happen to have my own, but finding + editing them would be a pain right now. This should give you an idea of how dynamic the cytoskeleton really is, though keep in mind it's not the best example by far. Noticed interesting recent developments in the plant cell morphogenesis/cytoskeleton story, wish I had time to keep up. (Source: Brandner et al. 2008 Plant Physiol Movie S1)

Now for the video of foram microtubules growing and fluorescing in vivo... oh wait, there is none. =(

There are no foram model organisms. Yet. As far as I know, there's no genome yet either. That should be taken care of. And someone needs to figure out how to transform/transfect (genetically) the buggers too. "Must have pretty movies of rapid microtubule growth" should look great on a grant app. Seriously, it's even shiny and glowy and stuff. Don't they like things that look like cancer/immunology research? (And this is probably why they don't let me write grants yet; not that I'm in any hurry to become a bureaucrat...)

Another foram teaser: some species (eg. Rotaliella heterocaryotica) possess two types of nuclei – germline and somatic – just like ciliates. Actually, no one has any idea how much like ciliates they are, as very little molecular work has been done. Might be another case of crazy genomic dimorphism with ridiculous epigenetic machinery, etc.

Or, just like forams themselves, it may be something else altogether.

References
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

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., ALEXANDER, S., STOCKTON, W., & DELACA, T. (1992). Extracellular Matrix Augments Mechanical Properties of Pseudopodia in the Carnivorous Foraminiferan Astrammina rara: Role in Prey Capture The Journal of Eukaryotic Microbiology, 39 (6), 724-732 DOI: 10.1111/j.1550-7408.1992.tb04455.x

Brandner, K., Sambade, A., Boutant, E., Didier, P., Mely, Y., Ritzenthaler, C., & Heinlein, M. (2008). Tobacco Mosaic Virus Movement Protein Interacts with Green Fluorescent Protein-Tagged Microtubule End-Binding Protein 1 PLANT PHYSIOLOGY, 147 (2), 611-623 DOI: 10.1104/pp.108.117481

Dupuy, C., Rossignol, L., Geslin, E., & Pascal, P. (2010). PREDATION OF MUDFLAT MEIO-MACROFAUNAL METAZOANS BY A CALCAREOUS FORAMINIFER, AMMONIA TEPIDA (CUSHMAN, 1926) The Journal of Foraminiferal Research, 40 (4), 305-312 DOI: 10.2113/gsjfr.40.4.305

Habura, A. (2005). Structural and Functional Implications of an Unusual Foraminiferal -Tubulin Molecular Biology and Evolution, 22 (10), 2000-2009 DOI: 10.1093/molbev/msi190