The Araeolaimida: We Barely Know Ye

Axonolaimus sera, from here.

Overall, the nematodes cannot be considered one of the best-known groups of animals. This is not because they are at all uncommon: there is the oft-cited factoid that nematodes are so abundant in every corner of the world that, if everything other than them was somehow instantaneously removed, the ghostly shadow of the planet Earth would supposedly still be visible as a cloud of microscopic worms. Nematodes are even found in places other animals are not: they have been found further beneath the Earth's surface than any other multicellular organism. There are some nematode species that attract attention, such as those that cause diseases, or are notable crop or animal pests. The nematode Caenorhabditis elegans has been a workhorse of developmental biology for many a year. But these well-studied taxa represent only a small proportion of the full nematode diversity out there.

Being very small and soft-bodied, nematodes do not usually present taxonomists with a great variety of clearly defined morphological features. As a result, dividing nematodes into well-supported groupings has not been an easy task (there are some notable exceptions: try looking up the Desmoscolecida one of these days). Take, as an example, the group known as the Araeolaimida. This name spent many years as a bit of a wastebasket for various non-parasitic nematode families. Eventually, it was restricted by Ley & Blaxter (2002) to just four families: the Axonolaimidae, Comesomatidae, Diplopeltidae and Coninckiidae, with many taxa previously treated as Araeolaimida included in a separate order Plectida. Fonseca & Bezerra (2012) include a fifth family, the Bodonematidae, that was not mentioned by Ley & Blaxter. Even in this restricted sense, the Araeolaimida may not represent a coherent group. There is no single feature shared by all araeolaimidans that is not found in other nematodes, and a molecular phylogenetic study of nematodes by van Megen et al. (2009) did not recover a monophyletic araeolaimidan clade. Nevertheless, Araeolaimida normally have the ovaries outstretched within the bodies of females (in many other nematode taxa, they are folded back on themselves), and the amphids (sensory grooves on the sides of the head) are usually spiral or looped in shape. The majority of araeolaimidans are marine, with freshwater and terrestrial environments being home to two genera of Diplopeltidae, and a few species of Axonolaimidae (Fonseca & Bezerra 2012). We don't know much about their diet, but they are probably grazers on micro-algae or bacteria. About 400 species of Araeolaimida have been described, but it would be very surprising if there weren't more out there.

Head end of the freshwater diplopeltid Cylindrolaimus, photographed by Peter Mullin. Note the dark circle near the end: this is the amphid.

The separate families are a bit easier to define (Fonseca & Bezerra 2012). The single known species of Bodonematidae, Bodonema vossi, stands out by having a pharynx with the mid-part differentiated into a series of muscular bulbs, as opposed to the fairly simple pharynxes of other Araeolaimida. Coninckia, the only genus of Coninckiidae, has the amphids sitting on differentiated plaques that are not present in other taxa. The Comesomatidae have spiral amphids, while the Axonolaimidae and Diplopeltidae have simpler looped amphids. The last two families are distinguished by the shape of the buccal cavity, which is larger and more strongly sclerotised in the Axonolaimidae.

One detail which caught my eye when researching this post is that males of some axonolaimids produce two different forms of spermatozoa (Riemann 1986). The sperm cells produced in the anterior testis of Nicascolaimus punctatus are more than three times the size of those produced in the posterior testis. In another axonolaimid species, Axonolaimus helgolandicus, it is the posterior testis that produces the larger cells. Both types of sperm were shown in N. punctatus to be transferred to females, but the reason for the two different sperm types is unknown. Pomponema, a genus belonging to a separate group of nematodes from the Araeolaimida, produces dimorphic sperm in which the larger cells seem to break down before they are transferred to the female, and it is possible that only one sperm type functions to fertilise the female in axonolaimids as well. Perhaps the other sperm type represent some sort of nuptial gift? Or could they somehow interfere with fertilisation by other males? We await the nematode enthusiast who will find out.

REFERENCES

Fonseca, G., & T. N. Bezerra. 2012. Order Araeolaimida De Coninck, 1965. Zoology Online. Berlin, Boston: De Gruyter. Retrieved 3 Jun. 2014, from http://www.degruyter.com/view/Zoology/HBZ-2011-000076.

Ley, P. de, & M. Blaxter. 2002. Systematic position and phylogeny. In: Lee, D. L. (ed.) The Biology of Nematodes, pp. 1-30. Taylor & Francis: Florence (Kentucky).

Megen, H. van, S. van den Elsen, M. Holterman, G. Karssen, P. Mooyman, T. Bongers, O. Holovachov, J. Bakker & J. Helder. 2009. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11 (6): 927-950.

Riemann, F. 1986. Nicascolaimus punctatus gen. et sp.n. (Nematoda, Axonolaimoidea), with notes on sperm dimorphism in free-living marine nematodes. Zoologica Scripta 15 (2): 119-124.

It's Nematodes All the Way Down

Halicephalobus mephisto, as illustrated by Borgonie et al. 2011.

It has to be said, nematodes are not among the most loved of organisms. For the most part, the only nematodes that get any press are either the developmental model animal Caenorhabditis elegans or the small proportion of species that affect us economically as parasites of ourselves or our food sources. There are not thriving clubs of amateur nematologists, there are no news-groups where nematode spotters eagerly spread the news of their latest desmoscolecid sighting. So it suggests something out of the ordinary may be going on when a new nematode species makes its debut in the pages of Nature, as one did today (Borgonie et al. 2011).

Appearance-wise, Halicephalobus mephisto is fairly ordinary (most nematodes are). It does have a higher-than-usual temperature resistance, being able to live in temperatures up to 41°C, but this is not extreme. Nor is the new species' ability to tolerate low oxygen concentrations, a common ability among minute animals such as nematodes and tardigrades. What is unusual about H. mephisto is where it was found: some 1.3 km beneath the surface of the Earth. Halicephalobus mephisto was recovered from fracture water (that is, water that was sitting in a fracture within the rock) in South Africa that had been isolated from the rest of the world for somewhere between 3000 and 12000 years, before being broken into by the Beatrix gold mine.

The presence of living organisms at this depth was not unexpected: bacteria had been found in fracture water previously. Nevertheless, this is the first time that a multicellular animal has been found at this depth. A samples taken in another mine at a depth of 0.9 km also recovered nematodes: one belonging to a previously known species, Plectus aquatilis, and one belong to an unidentifiable species of the family Monhysteridae. A sample taken at a depth of 3.6 km in a third mine did not recover any specimens, but did allow the recovery of nematode DNA suggesting their possible presence. Samples from the soil surrounding the boreholes from which the water samples were taken, as well as samples of the water used in drilling the mines themselves, were tested to establish that the nematodes were indeed from the original fracture water and not recent contaminants, but these control samples were nematode-free.

Halicephalobus mephisto lives a life completely isolated from the surface world, presumably feeding on the bacterial biofilms growing along the edge of the fracture. It would not be abundant: in the Beatrix mine sample, 6480 litres of water were filtered but only a single nematode was recovered (thankfully, the parthenogenetic nematode was successfully raised and bred in the lab, providing the necessary specimens for the species description). But it provides further support for the principal that where there is liquid water, there is life.

REFERENCE

Borgonie, G., A. García-Moyano, D. Litthauer, W. Bert, A. Bester, E. van Heerden, C. Möller, M. Erasmus & T. C. Onstott. 2011. Nematoda from the terrestrial deep subsurface of South Africa. Nature 474: 79-82.