Myxozoa

Introduction

Members of the Myxozoa are microscopic metazoan parasites with an extremely reduced body. The dimensions of the myxospore, the typical myxozoan stage in fish hosts, range usually between one hundredth and two hundredth of a millimetre. Myxospores consist of several cells, which are transformed to shell valves, nematocyst-like polar capsules with coiled extrudible polar filaments and amoeboid infective germs. Myxospores develop in plasmodia (trophozoites), which can be very large and polysporic (generally histozoic in host tissue) or small and mono- or disporic (coelozoic in organ cavities). Myxozoans are parasites of fish, worms (oligochaetes and polychaetes) and bryozoans. Few representatives were found as parasites of amphibians and reptiles, and recent findings confirmed the ability of myxozoans to infect mammals (Prunescu et al. 2007, Dyková et al. 2007) and birds (Bartholomew et al. 2008). Humans as potential hosts for myxosporea were also reported (Boreham et al. 1998, Moncada et al. 2001), however, myxospores were detected in faecal samples and probably just passed through the digestive tract.

Myxozoa Grassé, 1970 contains two classes: Malacosporea Canning, Curry, Feist, Longshaw et Okamura, 2000 and Myxosporea Bütschli, 1881. Malacosporea includes only two genera (Tetracapsuloides and Buddenbrockia) with a total of three described species. Myxosporea includes about 2200 species in 60 genera.

Wolf and Markiw (1984) discovered myxosporean life cycles altering between two host species – fish and annelid worm. The myxospore is ingested by annelids and then the myxosporean undergoes a schizogony and a gametogony. Finally, the parasite develops into an actinospore, a triradiate myxosporean spore, which infects the vertebrate host. Here, the sporoplasm released from the actinospore divides by endogony, and then presporogenic multiplication of the myxosporean occurs. The life cycle is completed with the development of mature myxospores in sporogonic plasmodia. The annelids are definitive hosts whereas vertebrates are intermediate hosts for Myxosporea.

Myxozoans were considered to be protists for more then one hundred years until the early nineties of 20^th century. Then, the phylogenetic analysis of the primal myxosporean SSU rDNA sequence (Smothers et al. 1994) confirmed earlier hypotheses that myxozoans are multicellular organisms (Štolc 1899, Weill 1938) and placed Myxozoa inside Metazoa. However, SSU rDNA data failed to find the correct position of the Myxozoa within metazoan taxa. Myxozoan SSU rDNA appeared to be a fast-evolving sequence resulting in long-branches in phylogenetic trees. Therefore, the SSU rDNA data are insufficient to decide whether Myxozoa are closely related either to Bilateria, Cnidaria (including Polypodium hydriforme) or other taxa (Smothers et al. 1994, Siddall et al. 1995, Hanelt et al. 1996, Siddall and Whiting 1999).

The rediscovery of Buddenbrockia plumatellae, a worm-like animal, as a myxozoan species was an important clue to the origin of Myxozoa (Monteiro et al. 2002). SSU rDNA of this enigmatic worm showed its close relationship to Tetracapsuloides bryosalmonae, and B. plumatellae was assigned to Malacosporea, the sister group to Myxosporea. Consequently Myxozoa were considered to be bilaterians or their close relatives (Monteiro et al. 2002). However, phylogenetic analysis based on sequences of numerous protein-coding genes (Jimenez-Guri et al. 2007) excluded a bilaterian origin of B. plumatellae and suggested Cnidaria as the most closely related taxon to Myxozoa.

The malacosporean Tetracapsuloides bryosalmonae and some myxosporean species are of economic importance causing significant losses of farm-reared fish. T. bryosalmonae causes dangerous proliferative kidney disease of salmonids (Kent et al. 1994). Probably the most serious myxosporean pathogen is Myxobolus cerebralis (whirling disease) which infects cartilage of freshwater salmonids and causes vast losses due to death (Nehring and Walker 1996). The other economically important species are e. g.  Enteromyxum leei (enteromyxosis) (Palenzuela et al. 2002), Henneguya ictaluri (proliferative gill diseases) (Pote et al. 2000) and Kudoa thyrsites (post-harvest soft flesh) (Kent et al. 1994).

Discussion of Phylogenetic Relationships

Hypotheses of phylogenetic relationships of Myxozoa are based primarily on the SSU rDNA data. These molecular data helped to confirm the phylogenetic position of Myxozoa inside Metazoa, and they have been a useful tool in discovering the relationships among myxozoan subgroups. The increasing number of myxosporean SSU rDNA sequences and their phylogenetic analyses cast doubt on the traditional taxonomic scheme of Myxosporea. Phylogenetic trees reveal great discrepancies between current taxonomy based on spore morphology (Lom and Dykova 2006) and analyses of molecular data. Particularly, the broader phylogenetic study of Fiala (2006) showed six polyphyletic and two paraphyletic genera and only four myxosporean genera were monophyletic. Moreover, just a fraction of myxosporean species diversity has been sequenced, and there are no sequence data from two thirds of described myxosporean genera. The tree above is based on the SSU rDNA tree after Fiala (2006).

The phylogenetic analyses of myxosporean SSU rDNA revealed unexpected and surprising relationships, e. g. the very close relationship of five species each from different genera (Myxidium giardi, Hofferelus gilsoni, Chloromyxum sp., Zschokkella sp. and Myxobilatus gasterostei); nine Sphaerospora species with known SSU rDNA forming five unrelated lineages; many Myxidium and Zschokkella species branching in different places in the phylogenetic tree, etc. (Holzer et al. 2004, Fiala 2006).

Many polytomies and paraphylies are typical results of analyses of myxosporean phylogeny. It will be a difficult task to find out relevant morphological synapomorphies, which would define a group of phylogenetically closely related myxosporean species. Spores are an abundant source of morphological features, but they are not an appropriate tool for future taxonomic classification, because in the past these characters have been shown not to be congruent with phylogenetic relationships; while vegetative stages cannot offer a sufficient number of morphological characters for taxonomic classification. For instance, one of the current key diagnostic features of Myxosporea, number of polar capsules (PC), is relatively easily changed during evolution as witnessed by:

1. the occurrence of Chloromyxum spp. (4 PC) in several different positions on the phylogenetic tree among myxosporeans with 2 PC;
   
2. the placement of Thelohannelus spp. (1 PC) inside the Myxobolus (2 PC) clade with no close relation to Coccomyxa spp. (1 PC) and Auerbachia pulchra (1 PC), which branch near marine Myxidium spp. (2 PC);
   
3. the multiplication of PC in some Kudoa spp. – K. neurophila (5 PC), K. neothunni (6 PC), K. yasunagai (7 PC) and K. permulticapsulata (13 PC!).

This is in contrast to the multivalve-state of myxospores, which appeared only once in the evolution from a marine bivalvulid ancestor (however, the bivalvulid Sphaerospora dicentrarchi clusters inside the multivalvulid Kudoa spp.).  In the traditional classification, Multivalvulida and Bivalvulida represent the only two orders of Myxosporea. However, multivalvulid species constitute just a subgroup of the phylogenetically determined “marine clade”, which is together with its sister “freshwater clade” the main lineage in the phylogenetic tree of Myxosporea (Fiala 2006).

Other Names for Myxozoa

• Cnidospora
• Myxosporea
• Myxosporidia

References

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Pote, L.M., L.A. Hanson and R. Shivaji 2000. Small subunit ribosomal RNA sequences link the cause of proliferative gill disease in channel catfish to Henneguya n. sp. (Myxozoa: Myxosporea). Journal of Aquatic Animal Health 12: 230-240.

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Information on the Internet

• Myxozoan Network. A network for scientists involved with myxozoan research.
• When is a worm not a worm? When it's a jellyfish. University of Oxford press release about Jiménez-Guri et al. 2007.