PHYLUM ENDOMYXA – Diversity of Life

EUKARYA> CHROMALVEOLATA> RHIZARIAE> ENDOMYXA

Endomyxa (in-do-MIX-uh) is derived from two Greek roots that mean within (endon -ἔνδον) and and fungus (mykes -μύκης). The reference is to the fungus-like growth of the internal parasites that occur in this phylum.

INTRODUCTION TO THE ENDOMYXA

These are free-living or parasitic cells that produce reticulopods. Some of them cause significant economic loss by infecting animals (e.g. oysters) and plants (e.g. cabbages, beets, watercress, and potato). Others in this phylum live in soil, on mosses, and in marine and freshwater environments. Free-living taxa feed on bacteria, algae, fungi (especially fungal spores), and small animals (Bass et al. 2009). Molecular phylogenetics (Cavalier-Smith and Chao 2003) has identified four major groups of endomyxans, two of which are free-living (Gromiidea and Proteomyxidea), one is a parasite of plants (Phytomyxea), and one is a parasite of animals (Ascetosporea).

Gromia (Figure 1) is a large benthic marine with an organic test. It was originally considered to be a member of the Foraminifera (another rhizarian phylum) because of the external test and the reticulate pseudopodia characteristic of that group. Furthermore, it had an elaborate life cycle. Burki et al. (2002) showed convincingly that the organism was not a foram. Matz et al. (2008) describe observations of Gromia spherica, a large (up to 30mm in diameter protist) off of the Bahamas. They observed the cells on the sediment and double-grooved tracks in their wakes. They interpreted the grooves to be created as the cell floats just above the sediment surface and feeds on detritus. Such tracks also occur in the precambrian, well before the Cambrian explosion. Matz et al. (2008) argue that the trails were left by a Gromia ancestor rather that by an early bilaterian, as had been postulated. Indeed, they suggest that the Ediacaran fauna of the Precambrian may have been large amoeboid Gromia-like cells with quilted thecae, a view supported by Pawlowski and Gooday (2009).


FIGURE 1. A photograph of living Gromia showing the external organic test with a single opening from which filopodia emerge. The spherical test is about 30mm in diameter. Image from: Matz et al. (2008)	FIGURE 2. Left: Image of living Gromia moving across sediment surface. Right: Fossil traces from 1.8 billion year old rock. These images from Matz et al. (2008) were used to support their argument that the Precambrian trace fossils usually attributed to early bilaterian animals likely were Gromia-like protists.

Other free-living members of the endomyxans are naked with reticulate or filose pseudopodia. Filoreta, which can live in soil, fresh water, or marine environments, as a trophozoite is a small mobile amoeba with bacterivorous filopods. They then elaborate very fine filopodia that interconnect with other cells forming a net-like meroplasmodium (see Figure 3) that, in appearance, is reminiscent of nets produced by Chlorarachnion (Bass et al. 2009). Cells can coalesce (or undergo multiple mitoses without cytokinesis) and form more typical multinucleate holoplasmodia.

Vampyrella primarily lives in calm freshwater habitats where the relatively large cells resemble orange heliozoans when they assume a spherical shape in open water (Hess et al. 2012). In contact with a substrate, they form sheet-like extensions from which filopodia emerge (see Figure 4). As trophozoites, they feed mainly on algae by inserting a feeding haustorium into the algal cell and extract the cellular contents. After feeding, the vampyrellids form distinctive digestive cysts from which the trophozoite emerges. The trophozoite also can enlarge as a multinucleate plasmodium, presumably by multiple mitoses without cytokinesis.

The pathogenic taxa are plasmodial intracellular parasites of other eukaryotes. Parasites of animals, the Ascetosporea, once were treated as members of the old protozoan class, Sporozoa. The haplosporidians are intracellular parasites of marine invertebrates. They are united by producing a spore with a lid and a spindle that remains persistent in non dividing nuclei. Economically, the most important species in this group is Haplosporidium nelsoni, which infects oysters and grow as plasmodia in their cells causing significant mortality (Figure 5). Others in the genus Urosporidium infect clams and crabs. Some species of Urosporidium are hyperparasites and infect flukes and nematodes that parasitize crabs. A careful survey of more than just economically important marine invertebrates would likely increase the known diversity many times over.

Marteilia, also a parasite of many economically important oyster species, causes Abers Disease, a disease of the digestive gland, in Ostrea edulis (Balouet 1979). The suggestion of a sexual life history with an intermediate host has not been borne out. However, pieces of the life history suggest that certain plasmodia undergo meiosis and then shed spores into the marine environment, and presumably are picked up by a microcrustacean, which disperses the spores. Where sexual fusion or gametogenesis might occur in the life history is unknown.

Unlike the other members of this group, Paradinium manifests itself as an external sac on infected copepods (see Figure 7) and other crustaceans. Skovgaard and Daugbjerg (2008) describe the Paradinium trophozoite as 8-10μm long amoebae connected by filopodia and lying in the body cavity. The plasmodium then forms a spore-bearing sac (the gonospore) that attached to the outside of the animal. Spores mature into motile cells with heterodynamic flagella, a presumed dispersive/infective stage. Other details of the life cycle are unknown.


FIGURE 3. A photograph of living Filoreta in the net-like meroplasmodium phase. The size bar = 10μm Image from: Bass et al. (2009)	FIGURE 4. A photograph of living Vampyrella in its attached form with sheet-like lobopod-like extensions from which filopods emerge. The orange color is typical. The size bar = 100μm Image from: Hess et al. (2012)	FIGURE 5. An SEM photomicrograph of the distinctive lidded spore of Haplosporidium. Image from: Burreson and Reece (2006)


FIGURE 6. A photomicrograph of a Haplosporidium plasmodium in the tissues of an oyster from the Chesapeake Bay. Image from: http://www.vims.edu/env/research/shellfish/gallery.html	FIGURE 7. Photomicrographs of the gonosporeal sac of Paradinium on a copepod. Image from: Skovgaard and Daugbjerg (2008)	FIGURE 9. A section through the cortical parenchyma of a Brassica root. The infected cells are filled with the secondary plasmodium (text with tooltip) of Plasmodiophora. Image from the Systematic Biology Biodiversity Collection.

Plasmodiophorids are important pathogens of plants and other eukaryotes. The most well known member is Plasmodiophora brassicae, a species that causes club root in cabbages and their relatives. See the life cycle of Plasmodiophora brassicae (Figure 8). Resting spores in the soil can be infective for up to seven years. If one were to germinate near the root of a cabbage (or a cabbage relative), the biflagellate zoospore can invade a roothair cell and form a small plasmodium, which releases secondary zoospores into the soil. There, compatible mating types pair and fuse back to back. Note that the cells fuse, but the nuclei do not. The resulting binucleate cell becomes amoeboid and invades the root epithelium again. There, it works its way into the cortex of the root where it invades a cortical parenchyma cell. Nuclear fusion (karyogamy) may occur at this point. If so, the resulting diploid cell feeds on the parenchymal cell and becomes enlarged and multinucleate (secondary plasmodium; see also Figure 9). The resulting tumorous growth of cells in the root cortex eventually prevents water and food from moving up and down the plant, which then dies. At this point, the plasmodia in necrotic tissue likely undergo meiosis, cytokinesis, and spore formation.

Other economically important members of this phylum include Spongospora subterranea, the cause of powdery scab in potato and crook root of watercress. Polymyxa betae infects sugar beet and facilitates the entrance of a virus. Together, they cause rhizomania of sugar beet. Furthermore, Polymyxa betae seems to behave as a vector for viruses in potatoes, watercress, and some cereal crops.

FIGURE 8. Details of the P. brassicae life cycle as described in the text.
This image was taken from: http://www.biologie.tu-dresden.de/botanik/LS/Physiologie/Life%20cycle.jpg

SYSTEMATICS OF ENDOMYXA

These taxa were considered to be amoebae, sporozoans, water molds, and slime molds at different times in recent history (see Margulis and Schwartz 1999). Patterson (1999) listed many of these taxa among the systematic orphans. Early work established the Rhizariae and the Cercozoa (Kuhn et al. 2000; Wylezich et al. 2002; Archibald et al. 2003; Longet et al. 2003, Nikolaev et al. 2003; Cavalier-Smith and Chao 2003; Archibald and Keeling 2004; Nikolaev et al. 2004; Bass et al. 2005). The relationships within the Endomyxa were slower in their development. Burki et al. (2002) established that Gromia was a relative of the cercozoa, and Cavalier-Smith and Chao (2003) pointed to an unexpected association between Gromia and Ascetosporea. Cavalier-Smith (2002) and Cavalier-Smith and Chao (2003) also established the sister relationship between Ascetosporea and Phytomyxa and the overall structure of the Endomyxa, which they considered to be a subphylum of Cercozoa (e.g. Adl et al. 2005). Problems remain in the systematics of the group (Bass et al. 2009). In particular, Proteomyxidea appears to be paraphyletic. Furthermore, the analyses of Ishitani et al. (2011) suggest that Endomyxa is paraphyletic and Gromia and Filoreta occupy a half-way position between Endomyxa and Foraminifera + Radiolaria. With the realization that the relationships between these taxa are in flux, we give the generally-accepted phylogeny of the Endomyxa (Figure 10), which is based on Bass et al. (2009) and Chantangsi et al. (2010). Note that the major parasitic taxa (Phytomyxea and Ascetosporea) occupy different clades within the Endomyxa.

FIGURE 8. A cladogram based on Bass et al. (2009) and Chantangsi et al. (2010) showing a simplified view of the relationships between the major taxa of the Endomyxa (those taxa highlighted in the shaded box). The taxa that are underlined were formerly classified in the same Class (Proteomyxidea).

LITERATURE CITED

Adl, S. M., A. G. B. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson, J. R. Barta, S. S. Bowser, G. Brugerolle, R. A. Fensome, S. Fredericq, T. Y. James, S. Karpov, P. Kugrens, J. Krug, C. E. Lane, L. A. Lewis, J. Lodge, D. H. Lynn, D. G. Mann, R. M. McCourt, L. Mendoza, O. Moestrup, S. E. Mozley-Standridge, T. A. Nerad, C. A. Shearer, A. V. Smirnov, F. W. Spiegel, and M. F. J. R. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology. 52(5):399-451.

Archibald, J. M. and P. J. Keeling. 2004a. Actin and ubiquitin protein sequences support a cercozoan/foraminiferan ancestry for the plasmodiophorid plant pathogens. Journal of Eukaryotic Microbiology. 51(1):113-118.

Archibald, J. M., D. Longet, J. Palowski, and P. J. Keeling. 2003. A novel plolyubiquitin structure in Cercozoa and Foraminifera: Evidence for a new eukaryotic supergroup. Molecular Biology and Evolution. 20:62-66.

Balouet, G. 1979. Marteilia refringens – Considerations of the life cycle and development of Abers Disease in Ostrea edulis. Marine Fisheries Review. January-February 1979: 64-66.

Bass, D., D. Moreira, P. Lopez-Garcia, S. Polet, E. E. Chao, S. von der Heyden, J. Pawlowski, and T. Cavalier-Smith. 2005. Polyubiquitin insertions and the phylogeny of Cercozoa and Rhizaria. Protist. 156: 149-161.

Bass, D., E. E.-Y. Chao, S. Nikolaev, A. Yabuki, K. Ishida, C. Berney, U. Pakzad, C. Wylezich, and T. Cavalier-Smith. 2009. Phylogeny of novel naked filose and reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist. 160: 75-109.

Burki, F., C. Berney, and J. Pawlowski. 2002. Phylogenetic position of Gromia oviformis Dujardin inferred from nuclear-encoded small subunit ribosomal DNA. Protist. 153: 251-260.

Burreson, E. M. and K. S. Reece. 2006. Spore ornamentation of Haplosporidium nelsoni and Haplosporidium costale (Haplosporidia), and incongruence of molecular phylogeny and spore ornamentation in the Haplosporidia. Journal of Parasitology. 92(6): 1295-1301.

Cavalier-Smith, T. 2002a. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. International Journal of Systematic Evolutionary Microbiology. 52:297–354.

Cavalier-Smith, T. 2003a. Protist phylogeny and the high-level classification of Protozoa. European Journal of Protistology. 39:338-348.

Cavalier-Smith, T. and E. E. Chao. 2003a. Phylogeny and classification of phylum Cercozoa (Protozoa). Protist. 154: 341-358.

Chantangsi, C, and B. S. Leander. 2010. An SSU rDNA barcoding approach to the diversity of marine interstitial cercozoans, including descriptions of four novel genera and nine novel species. International Journal of Systematic and Evolutionary Microbiology. 60: 1962-1977.

Febvre-Chevalier, C. 1990. Heliozoa. In: Margulis, L., J. O. Corliss, M. Melkonian, and D. J. Chapman, eds. 1990. Handbook of the Protoctista; the structure, cultivation, habits and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. Jones and Bartlett Publishers. Boston. pp. 347-362.

Grell, K. G. 1973. Protozoology. Springer-Verlag. New York.

Hess, S., N. Sausen, M. Melkonian. 2012. Shedding light on vampires: the phylogeny of vampyrellid amoebae revisited. PLoS ONE. 7(2): e31165. doi:10.1371/journal.pone.0031165

Hine, P. M., R. B. Carnegie, E. M. Burreson, and M. Y. Engelsma. 2009. Inter-relationships of haplosporidians deduced from ultrastructural studies. Diseases of Aquatic Organisms. 83: 247-256.

Kudo, R.R. 1966. Protozoology. 5th ed. Charles C. Thomas Publisher. Springfield.

Kuhn, S., M. Lange, and L. K. Medlin. 2000. Phylogenetic position of Cryothecomonas inferred from nuclear-encoded small subunit ribosomal RNA. Protist. 151: 337-345.

Longet, D., J. M. Archibald, P. J. Keeling, and J. Pawlowski. 2003. Foraminifera and Cercozoa share a common origin according to RNA polymerase II phylogenies. International Journal of Systematic and Evolutionary Microbiology. 53: 1735-1739.

Matz, M. V., T. M. Frank, N. J. Marshall, E. A. Wonder, and S. Johnsen. Giant deep-sea protist produces bilaterian-like traces. Current Biology. 18: 1849-1854.

Nikolaev, S. I., C. Berney, J. Fahrni, I. Bolivar, S. Polet, A. P. Mylnikov, V. V. Aleshin, N. B. Petrov, and J. Pawlowski. 2004. The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proceedings of the National Academy of Sciences. USA. 101(21): 8066-8071.

Patterson, D. J. 1999. The diversity of eukaryotes. American Naturalist. 154 (Suppl.): S96–S124.

Patterson, D. J. and M. Zölffel. 1991. Heterotrophic flagellates of uncertain taxonomic position. In: Patterson, D. J. and J. Larsen, eds. The Biology of Free-Living heterotrophic Flagellates. Clarendon Press. Oxford. pp. 427-475.

Pawlowski, J. and A. J. Gooday. 2009. Precambrian biota: protistan origin of trace fossils? Current Biology. 19(1): R28-R30.

Skovgaard, A. and N. Daugbjerg. 2008. Identity and systematic position of Paradinium poucheti and other Paradinium-like parasites of marine copepods based on morphology and nuclear-encoded SSU rDNA. Protist. 159: 401-413.

By Jack R. Holt. Last revised: 03/06/2013

PHYLUM ENDOMYXA (Cavalier-Smith 2002)

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