Eukaryotes are the branch of the tree of life with complex cells, containing a separate compartment for DNA, lots of internal compartments, and mitochondria that use oxygen to provide lots of energy. These features were so successful that we can't find any trace of a eukaryotic ancestor that lacks any of them. It has been suggested that the mitochondria's ability to mobilize energy was an essential ingredient for animal life.

That said, there are a small number of single-celled parasites that seem to have lost this energy-producing function over the course of evolution. They typically still have mitochondria-like compartments, but they've lost their DNA and role in aerobic metabolism. Instead, these compartments are involved in specialized chemical functions like producing hydrogen. But these were typically parasites that lived in oxygen-free environments and were only distantly related to animal life.

But now researchers have identified an animal that is also a parasite that lives in oxygen-poor environments. And it, too, has gotten rid of its mitochondria, being the first-known instance of an animal that lacks them.

The strange cousins we never talk about

A lot of animal life, including us and most of the animals we spend our time with, are bilaterians—they have a left and a right side. But there are plenty of organisms without this tidy body organization. Jellyfish, sea anemones, and corals belong to a separate branch of the animal kingdom called cnidaria. Cnidarians are typically radially symmetric and don't have a clear brain to coordinate their activities, but coordinate them they do, as the gentle swimming of jellyfish makes clear.

If these typical cnidarians strike you as a bit bizarre, the myxozoans are even further out past the borders of the familiar. They're obligate parasites, and their life cycle requires at least two hosts, typically a fish and a worm. Perhaps because of this specialized life cycle, there are actually a lot of them; scientists have described over 1,300 species so far. Although they don't infect humans (that we know of, at least), they do cause us problems, as their fondness for fish makes them a problem for commercial fish farms.

The only reason we've realized that these are cnidarians is that we obtained some DNA sequences from them. So, it's not too surprising that researchers have started sequencing the entire genomes of these organisms. The real surprise came when the researchers got to the genome of the species Henneguya salminicola, which, as its name implies, spends part of its existence preying on salmon. The discovery—or rather lack of discovery—was that it had no mitochondrial genome.

The mitochondria are the remains of what were once free-living bacteria, incorporated inside the cell and adapted for the production of the chemical energy source ATP. While many of the genes needed for mitochondrial function are found in the regular cellular genome located in the nucleus, the mitochondria retain their own genome, which still encodes a variety of proteins that are essential for its role in metabolism. It's difficult to see how the organism's mitochondria could function without a genome.

Myxed up myxozoans

To make sure there wasn't something strange about all myxozoans or their own lab procedures, the researchers sequenced the DNA from a related organism. The researchers found that the DNA had a perfectly reasonable mitochondrial sequence. They then looked at the nuclear genome sequence they'd obtained and looked for genes that would encode proteins needed for copying the mitochondrial DNA. While a related species had about 50 of these genes, Henneguya salminicola only had six. The gene encoding the actual enzyme that does the copying was there, but it had picked up three mutations that would leave it nonfunctional.

Searching for DNA inside the cell using a fluorescent molecule that sticks to it showed it was only in the nucleus of Henneguya salminicola. The related species had glowing mitochondria after being exposed to the dye. So, as best the researchers were able to tell, there were no mitochondria in this species.

So what’s that then?

Yet when the researchers looked using electron microscopy, they were able to see things that looked like mitochondria, having its typical layered membrane structure, including a series of folds in the innermost membrane. This is not completely unexpected; as mentioned above, some single-celled parasites that no longer have mitochondria that perform oxidative metabolism still build similar-looking structures that handle other metabolic functions.

To get a sense of what may be possible in Henneguya salminicola, the researchers looked for genes that encode components of the electron transport chain that helps make ATP. Most of those appear to be absent from this organism, indicating that whatever this structure is doing, it's not making ATP. In many of the single-celled parasites, the mitochondrial remnant releases hydrogen; the genes needed to do that appear to be absent as well. H. salminicola does, however, still contain genes needed for the metabolism that handles the building blocks of DNA, RNA, and proteins, suggesting that there are still some essential functions performed there.

So, the function of the mitochondrial remnant remains unclear at this point. But it is possible to speculate how this ended up being the only known animal species without functioning mitochondria. When in fish, the organism takes up residence in the white muscles, which apparently function using anaerobic metabolism. While it's not clear what the second host is, plenty of worm options also live in anaerobic environments. So, it's entirely possible that this organism was spending most of its existence without any oxygen to use for metabolism in the first place.

Parasitic species like Henneguya salminicola often lose features because the species they attack provides so much for them. If this organism rarely sees much oxygen, then losing the genes needed to perform oxygen-dependent reactions would be the expected outcome. It's also possible that having a smaller genome and less complicated internal structure would be evolutionarily favorable for these organisms.

Does this discovery mean that we should rethink the need for oxygen-based metabolisms as a prerequisite for animal life? Not entirely. It's pretty clear that these organisms would have a hard time surviving without animal hosts to provide many of the things we normally associate with more complicated organisms. So, it's entirely possible that the oxygen-based metabolism enabled by complicated cells remains essential for the origin of animals. It's only after those animals exist that it may be dispensable.

PNAS, 2019. DOI: 10.1073/pnas.1909907117 (About DOIs).