The return of Buddenbrockia

In a previous post I briefly mentioned the mysterious worm Buddenbrockia plumatellae Schröder 1910, listed by Haszprunar et al. (1991) as an "extant problematicum", and alluded to how the true identity of this critter was rather unexpectedly resolved a few years back (Okamura et al., 2002). Further work on the position of Buddenbrockia appeared this past Friday in Science and adds a further small twist to the tale (Jiménez-Guri et al., 2007).

Buddenbrockia is a parasite of freshwater bryozoans, small, sessile, colonial animals that are sometimes referred to as 'moss animals' for little apparent reason ('moss animals' happens to be the English translation of 'Bryozoa'). After Schröder first described it in 1910, he suggested two years later that it was related to nematodes due to its mesodermal muscle blocks. A relationship to trematodes (flukes) was suggested around the same time by Braem (Okamura et al., 2002).

Okamura et al. (2002) examined the ultrastructure of Buddenbrockia, and found that it possessed an inner and outer layer of cells separated by the aforementioned muscle blocks, of which there are four arranged around the body. There is no through gut. Most significantly, the outer cell layers (the mural cells) contained polar capsules. Polar capsules are rounded organelles containing a tightly coiled filament that can be ejected at great speed. The polar capsules of Buddenbrockia were very similar to those of Tetracapsula, a basal member of the Myxozoa (and also a bryozoan parasite).

In my earlier post, I referred to Myxozoa as the least animal-like of animals, and I unreservedly stand by that statement. Myxozoa are parasites and fall into two classes. The class Malacosporea contains the aforementioned Tetracapsula (and now Buddenbrockia) and are parasites of bryozoans and fish. The class Myxosporea is considerably larger and are parasites of fish and annelid worms. As an interesting aside, the Myxosporea was previously divided between two classes of superficially very distinct appearance, the fish-parasitic Myxosporea and the annelid-parasitic Actinosporea. This distinction was removed in the mid-1980s when it was shown that spores of the myxosporean Myxobolus fed to tubificid annelids developed into the actinosporean Triactinomyxon (Wolf & Markiw, 1984). The two 'classes', therefore, represent different stages in the myxosporean life cycle.

So derived are myxosporeans relative to other animals that until fairly recently they were not even recognised as animals at all, being instead classified with the parasitic protozoa (Sporozoa and Microsporidia). Myxosporeans contain very few cells, and are contained completely within the cells of the host for part of the life cycle. A connection with animals was first suggested on the basis of the presence in myxosporeans of collagen, and on the near-identical ultrastructure of the myxosporean polar capsule with the cnidarian nematocyst (stinging cell) (see here for more details).

Even after myxozoans were recognised as animals, however, their position within the animal kingdom proved very hard to establish. Obviously, the ultrastructural similarities supported a connection with the cnidarians (the parasitic cnidarian Polypodium [not to be confused with the fern genus Polypodium] was particularly suggested as a close relation). However, some molecular studies supported a connection with bilaterians, most notably the reported presence in myxozoans of bilaterian-like Hox genes.

When Okamura et al. (2002) published their ultrastructural study of Buddenbrockia, they felt that its worm-like structure supported a bilaterian relationship for myxozoans, and highlighted previous molecular studies connecting myxozoans to nematodes. Jiménez-Guri et al.'s (2007) publication, however, turns this on its head, and returns Myxozoa to a position with the Cnidaria. This was done through a Bayesian phylogenetic analysis of some 129 proteins in 47 animals (plus 13 opisthokont outgroups) in a range of higher taxa. Buddenbrockia proved to have a significant branch length (easily the longest on the tree). interestingly, parsimony analysis (which is very vulnerable to long-branch attraction) of the data set resulted in Buddenbockia associating with a clade of nematodes + platyhelminthes, the other long-branch taxa analysed. It is likely that long-branch attraction has also been the culprit for such associations in the past.

And those bilaterian-like Hox genes? Well, the authors of the current study managed to isolate the supposed myxozoan Hox genes from host species that were not even infected with myxozoans. They were unable to isolate them from myxozoan samples that had been scrupulously cleared of any host tissue. Therefore, the supposed myxozoan Hox sequences represent contamination from the hosts, and are not myxozoan at all.

REFERENCES

Haszprunar, G., R. M. Rieger & P. Schuchert. 1991. Extant "problematica" within or near the Metazoa. In The Early Evolution of Metazoa and the Significance of Problematic Taxa (A. M. Simonetta & S. Conway Morris, eds.) pp. 99-105. Cambridge University Press.

Jiménez-Guri, E., H. Philippe, B. Okamura & P. W. H. Holland. 2007. Buddenbrockia is a cnidarian worm. Science 317: 116-118.

Okamura, B., A. Curry, T. S. Wood & E. U. Canning. 2002. Ultrastructure of Buddenbrockia identifies it as a myxozoan and verifies the bilaterian origin of the Myxozoa. Parasitology 124: 215-223.

Wolf, K., & M. E. Markiw. 1984. Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225: 1449-1452.