Return of the Microscopic Parasitic Jellyfish

Myxozoan infesting salmon has degenerated so far it even lost the genes for breathing, Israeli and American scientists discover

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Fluorescence micrograph of spores of the parasitic cnidarian Henneguya salminicola. The fluorescent dye has penetrated the spore nuclei and membranes
Fluorescence micrograph of Henneguya salminicola sporesCredit: Stephen D. Atkinson

Animals breathe oxygen. This is a given. Until now, precisely three exceptions to that law of nature have been found and all three are loriciferans (tiny organisms found on the Mediterranean seafloor). Now a fourth animal has been identified that scorns respiration, and it’s a microscopic parasitic jellyfish that infests salmon.

In the case of myxozoan Henneguya salminicola, it even lost the genes that would have enabled it to breathe oxygen, an international team with Dorothée Huchon of Tel Aviv University, Stephen Atkinson of Oregon State University and others reported in the Proceedings of the National Academy of Sciences on Monday.

The microscopic parasites infesting marine life had been known to science for a long time, but their classification was a mystery. Ultimately, genetic analysis proved that the enigmatic parasites were actually jellyfish. This outcome absolutely stunned biologists on the grounds that the animals had lost their jellyfish characteristics to a degree that hadn’t been thought likely or even possible. They had retained some cnidarian-specific genes, on which their identification was based.

Myxozoans are a rare case of evolution from complex to simple – and an extreme one. It would be like finding a one-celled creature and discovering that, genetically, it’s a mammal.

You might not appreciate them, but jellyfish are complex beings. Forget cave fish that lost their eyes: the ancient group of myxozoans reverted to being effectively unicellular or a clump of cells, with the smallest genome known so far.

Light microscope image of spores of the parasitic cnidarian Henneguya salminicola, from Chinook salmonCredit: Stephen D. Atkinson

Also, the horrifying little endoparasites are anything but rare. In fact, a paper from 2018 estimates that myxozoa represent at least 20 percent of the phylum Cnidaria, which includes jellyfish, sea anemones and coral.

And they even exist on land: their homeothermic terrestrial victims include several shrew species, such as the Hungarian pygmy shrew, and waterfowl, such as the Pekin duck. Wouldn’t you know it would be this bunch that would lead the Cnidarians out of the water, no longer constrained to the aquatic environment. The myxozoan spores grow in the shrews’ livers, but happily the rodents seem to evince little suffering from the infection.

But now the Israeli-American team has found the weirdest myxozoan yet.

‘This is strange’

Animal cells contain mitochondria – organelles that have their own DNA, separate from the nuclear DNA. (Biologists suspect that mitochondria originated in bacteria that were “swallowed” by ancient single-celled critters billions of years ago and became incorporated into the cytoplasm.) Mitochondria produce energy for the cell by creating molecules called ATP (adenosine tri-phosphate) by a process called cellular respiration.

Some single-celled protozoans (which are short of being proper animals) adapting to low-oxygen environments secondarily lose aerobic respiration, replacing standard mitochondrial breathing with anaerobic metabolic mechanisms. But among proper animals, of which jellyfish are one, a fully anaerobic existence is unknown except in the case of the three loricifera species living in the sediment of a saline “lake” at the bottom of the Mediterranean. The loriceferans are less than a millimeter in size.

Also, some complex (and very small) animals can live in a very oxygen-deprived environment for some time, but they can and do enjoy oxygen when it’s available, Huchon explains.

Not this one. Just as extraordinary, the micro-jellyfish that doesn’t breathe was discovered by pure accident.

On sabbatical at co-author Stephen Atkinson’s lab, Huchon – who studies the evolution of the mitochondrial genome – was working on myxozoan samples and wound up sequencing H. salminicola by chance, she relates.

The data showed no mitochondrial genome. “I was very surprised,” she says.

Glowing dots: nuclear DNA in salminicola. There is no mitochondrial DNA, which would have appeared as much smaller blue dots.Credit: Stephen D. Atkinson

At first, Huchon assumed the missing mitochondrial DNA was an artifact of the software. In principle, each cell contains one nucleus with nuclear DNA and multiple mitochondria, even hundreds or thousands – each with mitochondrial DNA. Your heart cells each contain about 5,000 mitochondria, for instance. The software was programmed to remove repetitive elements, so sometimes the mitochondria genome gets eliminated from the data because it was repeated, Huchon explains.

“Then I started to look in detail and saw all the enzymes working with the mitochondrial genome were absent too. ‘This is strange,’ I said to myself. I looked for genes involved in respiration and they were gone too,” she relates.

There is no molecular data for the three nonbreathing loricifera found so far because retrieving them intact enough from the depths of the Mediterranean has been impossible, she explains. So the team’s findings were unprecedented.

As a control, the team analyzed a different myxozoan, Myxobolus squamalis, that infects trout and salmon in the Pacific Northwest. It has mitochondria with genomes, as mitochondria should.

The ultimate parasite

So how does H. salminicola breathe? “We don’t know,” Huchon answers candidly. “I don’t think the animal breathes at all. It’s a parasite and there are parasites that don’t breathe. Fungi, for example. They get energy from another source. One possibility is that they can steal the ATP molecules from the host. Steal ATP from the salmon.”

Salminicola even seems to grow backward, using the yardstick of more familiar development processes. At its first stage of life, the spore, H. Salminicola is multicellular. As they “grow up,” the cells fuse to create an effectively unicellular jellyfish – a single cell encased in a single membrane with multiple nuclei inside.

Actually, cellular fusion is not that unusual. Primitive fungi are essentially just big cells with a lot of nuclei inside, Huchon says. Some of our long muscle cells are fused multinucleated cells, which create each long muscle fiber.

Unlike our muscle cells, H. salminicola make cysts inside salmon. Asked if salmon imported to Israel might be infected with this extreme parasite, Huchon answers that they probably aren’t, because fish-eating shoppers would have noticed: H. salminicola cysts manifest as “disgusting white dots” in the pink salmon flesh that are definitely not microscopic. The condition is known as “tapioca disease.”

Salmon infected by Henneguya salminicola ("tapioca disease")Credit: Flying Penguin, Wikimedia commons

It seems most people have a simple view of evolution, Huchon says: that animals “should get more and more complex. These went the opposite way – to the simplest possible. Yet they are still successful because they can reproduce very quickly.”

The myxozoan salminicola has the simplest genome known yet – even simpler than that of its many, many brethren in the microscopic parasitic jellyfish tree – because it even ditched its mitochondria and mitochondrial breathing machinery. As Huchon sums up: “The paradigm can be simple and still be successful.”

Mitochondrial Related Organelles in salminicola that had infected a Chinook salmon.Credit: Stephen Atkinson & Teresa Sawyer
Spores of the parasitic cnidarian Henneguya salminicola, from Chinook salmonCredit: Stephen D. Atkinson