Ornamented spores produced by jellyfish descendants inside invasive cane toads in Australia. SEM photograph; scale bar 5 micrometers. Fig. 4 from Hartigan et al. 2011.

Once upon a time, a jellyfish became a parasite, and its descendants became unrecognizable.

Several are worms. Most are microscopic shapeless sacs. They produce spores, a behavior almost of unheard of among animals, and pass the majority of their lives freeloading inside animals.

Taken together, they look and act an awful lot like protists – microbes that swarm in ponds, in soil, and sometimes in bloodstreams (think malaria). They were mistaken for such for over 100 years. But I’d wager 99% of protists do not have ancestors that were large, free-living animals. These do.

And they are legion: some 2,000 species exist today. Now, thanks to a new study, we can state with more confidence than ever that they are all related to one another, and, in spite of their radically altered appearance, are indeed cnidarians -- the giant and ancient group of organisms that includes coral, jellyfish, sea pens, hydras, and sea anemones.

But you would never know it to look at them. Called myxozoans, they are wonderfully weird.

Star Spores and Whirling disease

Myxobolus cerebralis is a typical myxozoan. It causes whirling disease in juvenile salmon and trout, an ailment that leads hapless fish to swim in circles and warps their bodies, spines, and nervous systems.

The disease is yet another epidemic created when humans introduced an alien species to a new environment – in this case, dumping brown trout into the lakes and rivers of North America. Our native trout have little resistance to the disease the browns brought with them.

The parasite lives in the bones and cartilage of infected trout, where they produce pumpkin-seed shaped myxospores. When the fish dies, the spores disperse. The fortunate ones find themselves swallowed by Tubifex tubifex, the delightfully named annelid "sludge worm", a repulsive and puzzling mass of which I blogged about ages ago during my first few months as a blogger.

After establishing itself, it grows actinospores (“star spores”), fascinating jack-like structures evolved to acquire a new fish host and then insert their contents into it.



"Fdl17-9-grey". Licensed under Public Domain via Commons.

Three long bow-like arms that act as grappling hooks are fused to a central injection spike. Inside the tip of the spike are three “polar capsules” fitted with inside-out tubes capable of firing into fish. Once everted, a sticky coating on the tube helps secure the connection. A mass of infective amoeba-like cells called “sporoplasm” crawl into the host via the new docking port. From there, they travel to the host’s cartilage, where they form sacs of cells that cripple the fish.



"Actinomyxon" by The original uploader was JohnOwens at English Wikipedia - Transferred from to Commons.. Licensed under Public Domain via Commons.

These sacs later build the myxospores that infect sludge worms once more. Myxospores, too, contain two polar capsules. They are enclosed within two shell-like valves which may confer great longevity on the spores.

The myxospores of M. cerebralis inside a fish host. Note the two dark polar capsules in each spore. Dr. Thomas L. Wellborn, Jr., Click here for source and permission.

A sketch of the same myxospores, showing the polar filaments coiled up inside each polar capsule inside the two valves of the spore. Dr. Thomas L. Wellborn, Jr. Click here for source and permission.

The myxospores of M. cerebralis can survive at least three months at -20°C, and decades under typical conditions. When ingested by a sludge worm, the polar capsules fire into the worm’s gut lining, injecting their payload into the worm as deftly as the fish.

The Jellyfish That Turned Itself Into a Worm

Most other myxozoa differ in little but details from M. cerebralis. Most attack fish, although a few attack turtles, amphibians, or one lucky mammal: the common shrew. Myxozoa must also have an alternate invertebrate host – an animal whose body they must pass through developmentally before they can re-infect their preferred vertebrate. That alternate host is usually an annelid worm, of which earthworms are the most familiar example (but deep-sea tube worms are too).

Most spend their lives only a few cells big. They exist as shapeless sacs of cystoplasm filled with nuclei or amoeba-like cells that occasionally blossom into resilient or beautiful spores. M. cerebralis follows the typical myxozoan pattern: a different spore type in each host. Myxozoan spores are so different that they were once thought to belong to two entirely different taxonomic groups.

The vertebrate-infecting spore (the “myxospore”) usually contains one or two amoeba-like infective cells and two to seven polar capsules. It’s made of two valves joined by sutures and can take on many odd shapes, having in various species wing-like flanges or ridges (see image at top of post). Or it may be smooth as in M. cerebralis. The invertebrate spores tend to be star-shaped, as we have seen.

But not all myxozoans remain simple. I have written about this group before (“The Jellyfish That Conquered Land – and Australia”), and covered the accumulating evidence that they are indeed “degenerate” cnidarians. In that post I also wrote about the peculiarities of the most extraordinary myxozoan of all – Buddenbrockia.

Buddenbrockia is a tiny worm containing four muscle bundles that run the length of its sides. Inside its invertebrate host, a little filter-feeding animal called a bryozoan (the other major myxozoan invertebrate host beside annelid worms), it is "highly active, with continuous and vigorous sinuous writhing." Once they abandon bryozoan, they continue to undergo "repeated coiling and straightening." Under the microscope, they look uncannily like a nematode worm -- a ubiquitous soil dweller and animal par excellence.

(A) Buddenbrockia inside its moss animal host. Scale bar, 40 micrometers. (B) Cross section; the four muscle blocks are marked (M). Notice no gut. Scale bar, 20 micrometers. (C) Scanning electron microscope image of a Buddenbrockia plumatellae worm doing nematode impression. Scale bar, 100 micrometers. Figure from Jimenez-Guri et al. 2007.

Yet Buddenbrockia is not a nematode, or a worm of any kind we’ve seen before. It has no nervous system. No gut. No external sense organs. It does, however, have spores and skin armed with … polar capsules. And it is not alone. Worm-shaped myxozoa appear to have evolved (and devolved) several times.

What Are These Things?

For reasons that should be abundantly apparent by now, myxozoans have puzzled biologists for a very long time. Because they live like parasites and look like protists – i.e., microscopic and sparsely-celled -- that’s what biologists long assumed they were for more than 100 years. But there were clues to the contrary. Their spores were multicellular, for one. Their cell-to-cell junctions are of a type found only in invertebrates. And those characteristic polar capsules, though they appeared in organisms only a few cells big or shaped like a worm, were very reminiscent of something … the nematocysts of cnidarians.



"Nematocyst discharge" by The original uploader was Spaully at English Wikipedia - Transferred from to Commons.. Licensed under Public Domain via Commons.

In the last few decades, genetic evidence also began to suggest myxozoans were not protists, but animals of some sort … possibly the sister to an oddball cnidarian called Polypodium hydriforme. Other studies suggested a different placement, not as a cnidarians, but as a sister group to the bilaterally symmetrical animals (everything with a right and left side, and a few things without them like starfish and sea urchins, whose larvae still have right and left sides).

To help confirm that myxozoans are indeed cnidarians, and also to investigate what took place genetically during the transition from jellyfish to microparasite, a team of US, Israeli, and French Canadian scientists recently compared the whole genomes of several myxozoans, a strange cnidarian parasite called P. hydriforme, and a bunch of other cnidarians and animals.

P. hydriforme, while not a myxozoan, is a parasite of sufficient bizarreness to both rival Buddenbrockia and warrant brief mention here.

A String of Tentacly Pom-Poms

It parasitizes the eggs of sturgeon and paddlefish, primitive looking fish whose eggs are also valued by humans. You may know them better as caviar.

Since the animal lives inside a single cell – the egg – it is also the only known cnidarian that can live inside another cell, and one of very few animals that can do the same.

P. hydriforme begins life in its egg host as a single cell, but it grows into an inside-out larva. By inside-out, I mean that the digestive cell layer is on the outside of the animal and the skin-like cell layer is on the inside. This makes sense for a parasite; when bathing in one’s food, one wants maximum surface area for grazing.

Eventually, though, the fish prepares to spawn. When P. hydriforme senses its free ride is over, the whole organism everts, dramatically revealing a spiky clutch of tentacles, a working mouth, and a gut. And there isn’t just one of these. There’s a whole chain, a string of tentacly pom-poms called a stolon.

"Polypodium hydriforme. A) Stolon stage just after emerging from the host oocyte. B) Four specimens of free-living Polypodium with 12 tentacles. Photos by E. Raikova." Fig. 1 from Evans et al. 2008.

Once ejected into water, the stolon fragments into individual jellyfish-like forms. These reproduce asexually by cloning until they finally form gonads and gametes that re-infect young female fish.

Like the myxozoans, people have argued about exactly what P. hydriforme is. Unlike myxozoans, “cnidarian” has long been at the top of the list due to the obvious anatomical similarities. When scientists compared the DNA sequences of a protein long considered to be highly revealing of evolutionary relationships – 18S ribosomal DNA -- it was established as a probable cnidarian in a paper in BMC Evolutionary Biology in 2008.

Unlike the thousands of myxozoans, P. hydriforme is the lone example of its kind. In the new study, scientists compared the genomes and the “transcriptome” -- the set of all messenger RNAs created from the organisms’ DNA – of a sampler of myxozoans, P. hydriforme, and other cnidarians and animals. In animals, messenger RNAs often differ from the DNA they are created from because they are edited and spliced substantially during normal processing.

Using this data, they confirmed that myxozoans are cnidarians, and appear to be the sister group to P. hydriforme.

Family tree generated using anaysis of 51,490 amino acid positions and 77 groups of animals. You are located in "Deuterostomia" -- notice Homo sapiens. Ecdysozoa are insects, crustaceans, nematodes and the like. Porifera are sponges; Ctenophora are comb jellies. Fig. 2 from Chang et al. 2015.

Their data also indicated that P. hydriforme is myxozoans’ closest living relative; the parasite shared a more recent common ancestor with the myxozoans than any other living group. P. hydriforme, though large and complex, shares with the myxozoans the ability to parasitize fish internally, the same kind of nematocyst, and has similar minicollagen sequences, one of the gene types required to make nematocysts. Those polar capsules are indeed highly modified nematocysts co-opted not to attack and stun prey, but to attack and infect hosts.

Together, the evidence seems to suggest the endoparasitic lifestyle evolved just once in cnidarians. All descendents of the early parasitic pioneers ultimately shrank themselves almost beyond recognition, excepting only lonely P. hydriforme.

A Genome Stripped to Essentials

Further, the scientists’ genome and transcriptome analysis revealed that myxozoans’ degenerate “body” is mirrored by a massively degenerate genome – among the smallest of any animal. The genme of Kudoa iwatai, a myxozoan, is just 22.5Mb, compared to 561Mb in P. hydriforme and 1,005Mb in the tiny cnidarian Hydra. Kudoa has just 5,533 protein coding genes compared to Polypodium's 17,440 and Hydra's 16,839.

Moreoever, many genes involved in development, cell-to-cell communication, cell specialization, and in the shaping and building of body parts have been cast off.

Enrichment or depletion of expressed genes in different functional categories (GO = gene ontology). Myxobolus and Kudoa are myxozoans; the other three are "true cnidarians". Fig. 3 from Chang et al. 2015.

In other words, the genes necessary to build a large, complex animal – genes considered hallmarks of animals – are missing and presumed shed in the myxozoans. P. hydriforme, even though it is inarguably a parasite, still retains a gene complement and genome size similar to free-living cnidarians like the lab-rat Hydra. But it is also still a large, complex animal with, you know, body parts and stuff.

All this is not to say that our way is better and myxozons’s worse because they are “degenerate”. Rather, the differences – and the genetic changes that go along with them – reflect what is best for each way of life and are fascinating to see.

That we live on a planet where jellyfish can turn themselves inside out in the eggs of giant paddlefish, transform from pulsating bells into wriggling worms, or bid farewell to the ocean entirely and find themselves adrift on land in the bodies of cane toads or common shrews makes me happy beyond belief (although I’m sure I would not think so were I a shrew). Vive la difference.

References

Chang, E. Sally, Moran Neuhof, Nimrod D. Rubinstein, Arik Diamant, Hervé Philippe, Dorothée Huchon, and Paulyn Cartwright. "Genomic insights into the evolutionary origin of Myxozoa within Cnidaria." Proceedings of the National Academy of Sciences (2015): 201511468.

Hartigan, Ashlie, Ivan Fiala, Iva Dyková, Miloslav Jirků, Ben Okimoto, Karrie Rose, David N. Phalen, and Jan Šlapeta. "A suspected parasite spill-back of two novel Myxidium spp.(Myxosporea) causing disease in Australian endemic frogs found in the invasive cane toad." PLoS One 6, no. 10 (2011).

Jiménez-Guri, Eva, Hervé Philippe, Beth Okamura, and Peter WH Holland. "Buddenbrockia is a cnidarian worm." Science 317, no. 5834 (2007): 116-118.