Alfonsino Beryx splendens flesh infected by Kudoa thyrsites, from here.

Belongs within: Cnidaria.
Contains: Platysporina.

The Myxozoa are a group of parasitic animals in which the body has become greatly reduced to a small number of cells.

The return of Buddenbrockia
Published 9 July 2007

The mysterious worm Buddenbrockia plumatellae Schröder 1910 is among those animals listed by Haszprunar et al. (1991) as an “extant problematicum”. So it was certainly of interest when the true identity of this critter was rather unexpectedly resolved (Okamura et al. 2002). Further work on the position of Buddenbrockia by Jiménez-Guri et al. (2007) added a further small twist to the tale.

Buddenbrockia plumatellae individuals within their bryozoan hosts (left), mature worms filled with ovocytes (lower right) and section of a mature ovocyte (upper right), from Morris et al. (2002).

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).

I have elsewhere 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).

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.

Buddenbrockia: the gift that keeps on giving
Published 14 July 2007

After writing the above section just a few days ago, I learnt that I really should have held my tongue just a little longer. Another paper on Buddenbrockia (Morris & Adams 2007) makes the creature even cooler than I realised. Which is a big thing, because I already thought Buddenbrockia was a very cool little animal.

Firstly, I’ll briefly cover the ‘relationships of the Myxozoa’ section, because there’s not too much to say there. Morris and Adams support the idea of Buddenbrockia and Myxozoa as basal bilaterians, in a similar grade (though not necessarily clade) with Acoela and Mesozoa. However, they defer to past analyses in this, and their points against a cnidarian position for Buddenbrockia (primarily possession of muscle blocks and Hox genes) were both dealt with by Jiménez-Guri et al., with the former present in some cnidarians and the latter shown to be contamination (ironically, Morris and Adams note the similarity of one ‘myxozoan’ Hox gene to vertebrates and suggest the possibility of lateral transfer). That said, Jiménez-Guri et al. did not include any Acoela, which lie outside the Protostomia + Deuterostomia clade, in their analysis, and I feel that the possibility cannot be ruled out that their inclusion may have affected the result. As always in science, there is the prospect of further testing.

The really interesting part of Morris and Adams, however, lies in their detailed description of Buddenbrockia‘s development, which is bizarre and incredible and makes me all the more sympathetic to earlier researchers who did not even recognise myxozoans as animals. Buddenbrockia reproduces by means of spores (produced asexually, as far as I can tell—I haven’t come across any reference to cross-fertilisation methods) that accumulate in the central cavity of the worm until it bursts open, releasing the spores into the host’s coelom from whence they are ejected by the host into the surrounding water. It is not clear how exactly the spores infect a new host, but when we see them next they have hatched into unicellular amoeboids (the pre-saccular phase) within the basal lamina of the host. Note that I said unicellular—myxosporeans aren’t really ever unicellular in the strict sense but syncytial (large multinucleate mass without individual cells, also called plasmodial). Nevertheless, Buddenbrockia unicells do have only a single nucleus. Because of the laminal connection between individual zooids in Bryozoa, it is possible that Buddenbrockia infection can spread through a colony at this stage.

The unicells then push their way through the host muscle tissue and aggregate together under the peritoneum. And when I say aggregate, I mean they are packed. Morris and Adams use the term ‘pseudosyncytium’ to describes how the cells are pressed so close together that it becomes nigh on impossible to distinguish individual cells, if indeed they remain individual cells (Morris & Adams were unable to satisfactorily resolve this question). The host cells surrounding the pseudosyncytium react strongly, encapsulating the pseudosyncytium within cytoplasmic extensions and necrotic cells. It is from this ‘pseudocapsule’ as the authors call it that the mature worm develops.

Now comes one really cool point—this does not happen the same way in every host species. In most host species, the mature parasite develops muscle blocks and forms the worm-like form we’ve been discussing so far. In Cristatella, the muscle blocks never develop, and the mature Buddenbrockia forms an ovoid sac, the Tetracapsula form (believed once upon a time to be a separate taxon). Morris & Adams’ observations are of the worm form, and that’s what we’ll continue to explore.

Within the pseudocapsule, the individual unicells form junctions with each other, and start growing out into the host coelom as the ‘worm’. Fibres are extruded from the pseudosyncytium that anchor it to the surrounding host cells. Within the worm, the pseudosyncytial cells differentiate into an outer layer of ectoderm and two inner layers of mesendoderm. The worm hollows out as it grows and a fibrous lamina develops between the mesoderm and endoderm. The endoderm develops into spore-producing cells, while the mesoderm forms the muscle blocks.

The muscle blocks develop from the base of the worm at the pseudosyncytium. One of the more unusual suggestions about Buddenbrockia muscle develop is that it may involve the co-option of host myofibres. If correct, this suggestion may explain why Buddenbrockia doesn’t develop muscle tissue in all host species, as maturation of Buddenbrockia in Cristatella (as well as development of the closely-related Tetracapsuloides, which also doesn’t develop muscles) takes place entirely in the coelom rather than in the cell wall. It also correlates with Buddenbrockia‘s unusual develop of muscle blocks within already-differentiated mesoderm. However, Morris & Adams didn’t find any direct evidence for host co-option.

Eventually, the mature worm is released from the coelom wall to become the free worm we all know and love. Whether the worm is released from the pseudosyncytium which remains behind to generate other worms, or whether the pseudosyncytium comes free with the worm and is resorbed is currently unknown, though Morris & Adams cite past observations of worms with scalloped ends as suggesting the latter option.

As I already noted, the malacosporean (Buddenbrockia + Tetracapsuloides) lifecycle with multiple individuals coming together to form a single mature form is completely unlike any other class of animal. In many ways, it is more reminiscent of the slime moulds, a point noted by Morris & Adams, particularly the so-called ‘cellular slime moulds’. Cellular slime moulds are now regarded as forming two separate groups – the dictyostelids in Amoebozoa and the acrasids in Heterolobosea. Neither of these groups is related to myxozoans (or, for that matter, to each other), so this form of life cycle has evolved independently in all three. It would be fascinating to see if the separate unicells aggregating together all derive from a single infective spore multiplying at the unicellular stage, or whether the products of multiple infections with different genetic identities can form a single pseudosyncytium. Aggregation of different genetic ‘individuals’ can happen in slime moulds – such chimaeras seem to be at a functional disadvantage to genetically pure aggregates, but this may be compensated for by the ability to form a larger colony (Foster et al., 2002). For Buddenbrockia, living in a soup of host-supplied nutrients with no need to move particularly far, the functional restrictions on chimaera formation might be even less.

Systematics of Myxozoa
    |  i. s.: MyxosomaK-M02c
    |           |--M. cerebralisPHK96
    |           `--M. moroneK-M02c
    |         Tetracapsuloides bryosalmonaeBAH03
    |    |--Buddenbrockia plumatellae Schröder 1910OC02
    |    `--Tetracapsula [Saccosporidae]KA01
    |         |--T. bryosalmonae Canning et al. 1999 [incl. T. renicola Kent et al. 2000]KA01
    |         `--T. bryozoides (Korotneff 1892) [=Myxosporidium bryozoides]KA01
    `--Myxosporea [Actinosporea, Bivalvulida, Myxospora, Myxosporidia, Variisporina]OC02
         |  i. s.: Myxoproteus reinhardtiiK-M02d
         |         ChloromyxumKA01
         |         HoferellusKA01
         |           |--H. carassiiKA01
         |           `--H. cypriniKA01
         |         MyxobilatusKA01
         |         OrtholineaKA01
         |         Polysporoplasma sparisKA01
         |         Zschokkella novaKA01
         |         SiedleckiellaKA01
         |         Myxostoma cerebralisMS98
         |--+--+--‘Myxidium’ truttaeKA01
         |  |  `--Raabeia Janiszewska 1955KA01, KD02
         |  |       |--R. furciligera Janiszewska & Krzton 1973KD02
         |  |       |--R. gorlicensis Janiszewska 1957KD02
         |  |       `--R. magna Janiszewska 1957KD02
         |  `--+--PlatysporinaKA01
         |     `--+--SphaerosporaKA01
         |        |    |--S. dicentrarchiKA01
         |        |    |--S. oncorhynchiKA01
         |        |    |--S. renicolaKA01
         |        |    |--S. testicularisKA01
         |        |    `--S. truttaeKA01
         |        `--MyxidiumOC02
         |             |--M. bergenseK-M02a
         |             |--M. giardiKA01
         |             |--M. incurvatumK-MC02
         |             |--M. leeiKA01
         |             |--M. lieberkeuhniJ-GP07
         |             `--M. trachinorumOC02
            `--+--+--Parvicapsula minibicornisKA01
               |  `--KudoaKA01
               |       |  i. s.: K. cerebralisK=M02c
               |       |         K. ovivoraKA01
               |       |--+--K. amamiensisKA01
               |       |  `--K. crumenaKA01
               |       `--+--K. ciliataeKA01
               |          `--+--K. thyrsitesKA01
               |             `--+--K. miniauriculataKA01
               |                `--K. paniformisKA01
                         |--C. acadiensisK-M02a
                         |--C. diplodaeKA01
                         |--C. labracisKA01
                         |--C. macrosporaK-MC02
                         |--C. shastaKA01
                         |--C. sparusauratiKA01
                         `--C. urophysisK-M02a

*Type species of generic name indicated


[BAH03] Bahri, S., K. B. Andree & R. P. Hedrick. 2003. Morphological and phylogenetic studies of marine Myxobolus spp. from mullet in Ichkeul Lake, Tunisia. Journal of Eukaryotic Microbiology 50 (6): 463–470.

Foster, K. R., A. Fortunato, J. E. Strassmann & D. C. Queller. 2002. The costs and benefits of being a chimera. Proceedings of the Royal Society of London Series B—Biological Sciences 269: 2357–2362.

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

[J-GP07] Jiménez-Guri, E., H. Philippe, B. Okamura & P. W. H. Holland. 2007. Buddenbrockia is a cnidarian worm. Science 317: 116–118.

[KA01] Kent, M. L., K. B. Andree, J. L. Bartholomew, M. El-Matbouli, S. S. Desser, R. H. Devlin, S. W. Feist, R. P. Hedrick, R. W. Hoffmann, J. Khattra, S. L. Hallett, R. J. G. Lester, M. Longshaw, O. Palenzuela, M. E. Siddall & C. Xiao. 2001. Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48: 395–413.

[K-M02a] Klein-MacPhee, G. 2002a. Cods. Family Gadidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder’s Fishes of the Gulf of Maine 3rd ed. pp. 223–261. Smithsonian Institute Press: Washington.

[K-M02b] Klein-MacPhee, G. 2002b. Temperate basses. Family Moronidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder’s Fishes of the Gulf of Maine 3rd ed. pp. 374–389. Smithsonian Institute Press: Washington.

[K-M02c] Klein-MacPhee, G. 2002c. Righteye flounders. Family Pleuronectidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder’s Fishes of the Gulf of Maine 3rd ed. pp. 560–587. Smithsonian Institute Press: Washington.

[K-MC02] Klein-MacPhee, G., & B. B. Collette. 2002. Scorpionfishes. Family Scorpaenidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder’s Fishes of the Gulf of Maine 3rd ed. pp. 331–338. Smithsonian Institute Press: Washington.

[KD02] Koprivnikar, J., & S. S. Desser. 2002. A new form of raabeia-type actinosporean (Myxozoa) from the oligochaete Uncinais uncinata. Folia Parasitologica 49: 89–92.

[MS98] Margulis, L., & K. V. Schwartz. 1998. Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth 3rd ed. W. H. Freeman and Company: New York.

Morris, D. J., & A. Adams. 2007. Sacculogenesis of Buddenbrockia plumatellae (Myxozoa) within the invertebrate host Plumatella repens (Bryozoa) with comments on the evolutionary relationships of the Myxozoa. International Journal for Parasitology 37 (10): 1163–1171.

[OC02] 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.

[PHK96] Prescott, L. M., J. P. Harley & D. A. Klein. 1996. Microbiology 3rd ed. Wm. C. Brown Publishers: Dubuque (Iowa).

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.

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