Buddenbrockia: The Gift that Keeps on Giving

A few days ago, I commented on the recent publication by Jiménez-Guri et al. (2007) on the basal myxozoan and parasitic worm Buddenbrockia (I'd recommend reading that post before this one - see Pharyngula for another good post on the same paper). I really should have held my tongue just a little longer, because just today I received notice of yet another paper on Buddenbrockia (Morris & Adams, 2007), and it 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 - on PZ Myers' post linked to above, David Marjanović corrected him on the point that 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.

REFERENCES

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.

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

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.