Sunday Protist – Gromia: beautiful predatory grapes of the sea

And we're back. The protists and I, that is. Well, the protists never quite went anywhere but you know what I mean...

You may have heard of Gromia a couple years ago when it hit the news by leaving tracks on the ocean floor resembling Ediacaran trace fossils (tracks). Or perhaps not; I tend to get overly excited the one time a year some protist makes the news. The giant (3cm) track-leaving Gromia in question sounded even cooler as it came from the great deep sea; other species of Gromia are in fact quite content with the more familiar shallow waters as well, crawling on the holdfasts of kelp in addition to thriving in the ice cold polar waters of McMurdo Sound (Antarctica), where the vibrantly colourful first specimen below comes from:

Gromia, from various locales including Antarctica (A), Madeira in the Atlantic (B) and Guam (C). Big and colourful, what's not to like there? Scalebars: A - 1mm; B - 0.5mm; C - 0.1mm (Burki et al. 2002 Protist)

For some time, there has been considerable confusion between Gromia and the cruelly similarly-named foraminiferan Allogromia, bad enough to warrant a Nature paper (Hedley 1958). At first glance, they do appear somewhat similar: a sizeable grape-like blob of a test surrounded by a mass of fine pseudopodia. While foram pseudopodia form a rather elaborate and extensive network of doom and terror for anything they come in contact with, Gromia uses more modest non-fusing alternative of pseudopodia. Thus, prior to molecular data, it was often considered a sort of a precursor to the more grown-up real forams, and assumed to have a rather simple test. They could hardly be more wrong, both with the assumed relation to forams and the simplicity of its test.

Typically (using that word rather loosely), a protist test consists of the plasma membrane covered by some sort of an organic matrix (often sugary proteins and protein-y sugars), followed by the deposited structural material, be it agglutinated bits of rock from the environment (often carefully and specifically selected) or secreted calcium carbonate, siliceous scales or something else entirely. To my knowledge, the process of selecting material for the test in agglutinating species, and formation of the test in general, is still quite poorly understood. There is some understanding of how diatoms and some coccolithophorids build their extracellular wonders, but most amoebae have been largely ignored, even the more 'famous' representatives like the forams, euglyphids and arcellinids. The Allogromia mentioned earlier has the organic (non-calcified, non-agglutinated) test characteristic of Allogromiids at large, who form a vast paraphyletic sea of diversity from which the more popular lineages arise – the Protista of the foram world, if you will.

Gromia also carries an organic test, hence the confusion with Allogromiids. But its test turns out to be a bit more elaborate, with an inner lining consisting of up to ten layers of odd honeycomb membranes, the whole thickness of the structure penetrated by multitudes of pores. The test surface is sometimes covered by attached bacteria (Aranda da Silva & Gooday 2009 DSR II). Furthermore, rather than simply a hole in the wall, its opening is surrounded by a complicated oral capsule which acts as a valve or a trap door: when the pseudopodia are withdrawn, the opening closes. One seldom thinks of movable structural parts on the microscopic level, but here you go:

The structure of Gromia's test and oral capsule, in that order. The figure on the right shows a pseudopodium gradually protruding through the closed aperture. (Hedley & Bertaud 1962 J Protozool; Mazei & Tsiganov 2006 in Presnovodniye Rakoviye Amyobi (in Rus.))

The pores make the test surface look quite pretty in reflected light:

The giant deep sea Gromia sphaerica; note the complex test surface structure with prominent perforations. (Matz et al. 2008 Curr Biol)

To make these mysterious 'grapes' of the sea even sexier, they are known to have sex. Upon conjugation, flagellated gametes are exchanged between the parents, producing amoeboid diploid swarmers that ultimately form a new test and complete the cycle. The parental shell and all the work that went into building one is abandoned in this process. Both forams and gromiids are 'mortal' in our sense – they spend a period of time building a body that eventually becomes abandoned by the next generation. Organisms like many flagellates, for example, are somewhat 'immortal' in that the cell is never abandoned between generations, but rather split up and shared by mostly clonal offspring. Extra structural complexity often bears the curse of losing 'immortality'.

Gromia's life cycle. (Arnold 1966 J Protozool)

Gromia shares some strangeness with giant deep sea Xenophyophores (forams): they like to live in their own excrement. This may sound disturbing, but they're still fairly microscopic, so their shit is of a rather more chemical character. Curiously, both Xenophyophores and Gromia tend to lean toward the upper end of the protist size range, perhaps partly aided by their inability or lack of desire to part with their faeces – these faecal pellets, so-called stercomata, appear to play a structural role in the Xenophyophores, and may well contribute to structure in Gromiids as well. Waste accumulation is not too grave a problem for these organisms due to their habit of generating clouds of swarmers that ditch the parental shell forever.

As alluded to earlier, gromiids are fairly distantly related to forams, and definitely evolved their elaborate test independently. For some time, gromiids were thought to be closely related to filose amoebae with shells, ie cercozoan euglyphids and such. Turns out, while not too close to the euglyphids, Gromia is a cercozoan (Burki et al. 2002 Protist), and tends towards the endomyxean side with the plant parasite phytomyxids, vicious vampyrellid amoebae and the ornate haplosporidia. In other words, things that look little like them, aside from a tendency to form thin pseudopodia.

Gromiids probably have a bigger story to tell, as environmental sequence data reveal swaths of cryptic diversity, and new species are still being described from the deep sea as well as polar waters (eg. Rothe et al. 2009 Zool J Linn Soc; Gooday & Bowser 2004 Protist; Rothe et al. 2011 Polar Biol; and Aranda da Silva et al. 2006 Mar Biol for diversity porn). As for their ecological niche, the gromiids seem to play a similar role to allogromiids and other forams – versatile predators preying on algae and anything else that gets caught in their feet.

Aww, they even grow on trees! Gromia schmoozing with a tree-shaped foram, Pelosina, possibly in some sort of a symbiotic relationship. (Gooday & Bowser 2004 Protist)

Hopefully back to more regular blogging now. Quality of writing is at the mercy of my irritating writer's block, you have been warned...

References
Aranda da Silva, A., & Gooday, A. (2009). Large organic-walled Protista (Gromia) in the Arabian Sea: Density, diversity, distribution and ecology Deep Sea Research Part II: Topical Studies in Oceanography, 56 (6-7), 422-433 DOI: 10.1016/j.dsr2.2008.12.027

Silva, A., Pawlowski, J., & Gooday, A. (2005). High diversity of deep-sea Gromia from the Arabian Sea revealed by small subunit rDNA sequence analysis Marine Biology, 148 (4), 769-777 DOI: 10.1007/s00227-005-0071-9

ARNOLD, Z. (1966). Observations on the Sexual Generation of Gromia oviformis Dujardin The Journal of Eukaryotic Microbiology, 13 (1), 23-27 DOI: 10.1111/j.1550-7408.1966.tb01863.x

Zach M. Arnold (1952). Structure and Paleontological Significance of the Oral Apparatus of the Foraminiferoid Gromia oviformis Dujardin Journal of Paleontology, 26 (5), 829-831

BURKI, F. (2002). Phylogenetic Position of Dujardin inferred from Nuclear-Encoded Small Subunit Ribosomal DNA Protist, 153 (3), 251-260 DOI: 10.1078/1434-4610-00102

[Fuck this, the browser crashed TWICE and I'm not finding all the links again. Not tonight anyway. URLs are in the post.]