Friday 20 November 2015

Discovering the origins of Myxozoan parasites.

Myxozoans are parasitic Euaryotic organisms that typically have a two host life-cycle. In most forms this involves a stage which infects an invertebrate, often an Annelid Worm, and a stage which infects a vertebrate host, usually a Bony Fish. For example the Myxozoan Myxobolus cerebralis infects Tubifax Worms, Tubifex tubifex, producing a large number of infective actinospores which are capable of anchoring onto Rainbow Trout, Oncorhynchus mykiss. Once attached to a Trout host the actinospore injects its protoplasm into the host's tissue, where a second life-cycle stage develops, the Myxospore, incidentally causing Whirling Disease in the Fish (a disease that causes both deformation of the spine and neurological damage in growing Fish, causing them to 'whirl' when they attempt to swim). These myxospores are released into the water when the Fish dies (usually prematurely) and are eventually consumed by new Tubifex Worm hosts, and the cycle repeats itself.

Myxozoans were first discovered in the 1880s, and were assumed to be Protists, single-celled Eukaryotes such as Amoebae, though some species have been shown to produce multicellular stages as part of their life-cycle, for example some Malacosporean Myxozoans produce a vermiform ('worm-like') stage. However since the 1990s several genetic studies have suggested that Myxozoans might be descended from multi-cellular animals, with different studies recovering them as either members of the Cnidaria (the group that includes Jellyfish, Corals and Sea Anemones) or as the sister-group to the Bilateria (all animals except Cnidarisns, Sponges and Ctenophores – Sea Combs). This is not totally surprising, as parasites often show very reduced body-plans, losing the ability to perform functions they rely on their hosts to do as part of an evolutionary drive to reduce their body-size. Myxozoans also produce some proteins otherwise only known in Cnidarians, and the polar capsule used by the actinospore stage Myxozan to inject its protoplasm into a vertebrate host has been compared to the nematocysts (stinging cells) of Cnidarians, further supporting the idea that Myxoans and Cnidarians may be closely related.

In a paper published in the Proceedings of the National Academy of Sciences of the UnitedStates of America on 16 November 2015, Sally Chang of the Departmentof Ecology and Evolutionary Biology at the University of Kansas, Moran Neuhof of the Department of Zoology and Department ofNeurobiology at Tel-Aviv University, Nimrod Rubinstein of the Department of Molecular and Cellular Biology at Harvard University, Arik Diamant of the National Center for Mariculture at Israel Oceanographic and Limnological Research, Hervé Philippe of the Station d’Ecologie Expérimentale du Centre national de la recherche scientifique and the Département de Biochimie at the Université de Montréal, Dorothée Huchon, also of the Department of Zoology at Tel-Aviv University and PaulynCartwright, also of the Department of Ecology and Evolutionary Biology at the University of Kansas, describe a genetic phylogeny of the Myxozoa and Cnidaria developed using the complete genomes of two distantly related Myxozoans, Kudoa iwatai and Myxobolus cerebralis, plus the previously published genomes of three other Myxozoan species, Buddenbrockia plumatellae, Tetracapsuloides bryosalmonae, and Thelohanellus kitauei, as well as 23 species of Cnidarians and 38 representatives of other animal groups, plus nine unicellular Eukaryotes.

Myxobolus cerebralis alternates its development between a Fish (Salmonid) host and an Annelid (Tubifesx tubifex) host. The myxospore is produced in the Fish (Right), and the actinospore is produced in the Annelid (Left). Both stages consist of just a few cells, including those housing polar capsules. Chang et al. (2015).

Chang et al. paid particular attention to one particular Cnidarian, Polypodium hydriforme, which is highly unusual in that, like Myxoans, it is parasitic. Polypodium hydriforme has a two stage life-cycle, with a free living stage that resembles a small Jellyfish and a parasitic stage that infects the oocytes (unfertilized eggs) of Paddlefish and Sturgeon. This parasitic stage of Polypodium hydriforme resembles the stolon of Jellyfish, an attached Hydroid-like stage which hatches from eggs produced by the free-swimming Medusa stage Jellyfish. The stolon of Jellyfish grows attached to a substrate then divides asexually into numerous new Medusae, while that of Polypodium hydriforme develops within the oocytes of the Fish, then fragments into numerous new adults.

In Polypodium hydriforme, the stolon stage (Top) develops inside the ovaries of its host (Acipenceriform fish). Upon host spawning, Polypodium hydriforme emerges from the host’s oocyte (Right), fragments, and lives as a free-living stage with a mouth (Left) before infecting its host. Chang et al. (2015).

Previous studies of Cnidarian phylogeny have suggested that Polypodium hydriforme is a sister-group to the Medusozoa (Jellyfish), i.e. all Jellyfish share a common ancestor more recent than their last shared ancestor with Polypodium hydriforme, but that that shared ancestor lived more recently than the common ancestor of the Medusozoa and any other known Cnidarian group.

Chang et al.'s findings support the close relationship of Polypodium hydriforme and the Medusazoa, but place the Myxozoa within the Cnidaria as the sister-group to Polypodium hydriforme; i.e. the most recent common ancestor of all known Myxozoans lived more recently than the common ancestor of Myxozoans and Polypodium hydriforme, and that shared ancestor had a shared ancestor with the Medusazoa more recently than with any other Cnidarian group.

Phylogenetic tree generated from a matrix of 51,940 amino acid positions and 77 taxa using Bayesian inference under the CAT model. Support values are indicated only for nodes that did not received maximal support. Bayesian posterior probabilities/ML bootstrap supports under the PROTGAMMAGTR model are given near the corresponding node. A minus sign (‘‘−’’) indicates that the corresponding node is absent from the ML bootstrap consensus tree. Chang et al. (2015).

This analysis supports the idea that the Myxozoans are Cnidarians, but it also implies on some very long gaps in the evolutionary record, and such gaps can be problematic; when looking at the relationships between distantly related groups without intervening taxa the limited amount of data can be misleading, resulting in false conclusions.

To try to overcome this problem Chang et al. next looked at the surviving genes in the Myxozoans examined. Just as the morphology of parasites is often greatly simplified, so they tend to lose much of their genetic heritage, with genes and gene-families which code for functions no longer performed by the parasite. Myxozoans have genomes comparable with the simplest other animal genomes yet described, those of parasitic Nematodes. Chang et al. found that Myxozoans have lost most of the genes used for body patterning, cellular differentiation and intercellular communication, though these are still present in Polypodium hydriforme, but other gene-families, such as those involved in stem-cell differentiation were still present, and showed clear affinities to those of other Cnidarians.

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