It was the greatest leap in evolution since the emergence of life on Earth. So-called eukaryotic cells, the building blocks of all multicellular organisms like you and me, animals, plants, fungi, and also a whole zoo of single-celled protists, evolved from a common ancestor more than a billion years ago. This ancestor resembled current-day prokaryotes, i.e. bacteria and archaea. These organisms populated all imaginable habitats and developed a plethora of wildly diverse means of obtaining their energy. However, the simple structure of their cells limited their size and complexity of interactions. With time, our ancestor developed a series of innovations that are nowadays defining characteristics of the eukaryotic cell. How this process went through, what was its driving force, and in what order those particular steps took place still remains a question provoking lively discussions among scientists. However, regardless of the details, among the most crucial steps in forming a eukaryote was undoubtedly the acquisition of a mitochondrion.

Today, mitochondria are small organelles within our cells that form complex and ever-changing networks. The sausage-shaped mitochondria constantly split, merge, and move around in order to provide all cellular regions with a life-giving chemical energy. This energy, produced on the inner surface of mitochondria, is produced by reactions between the nutrients we get from food and the oxygen we breathe in. Cells can produce energy also without the help of mitochondria and many organisms which live in oxygen-poor environment indeed do so, but the mitochondrial energy production is more than ten times more efficient. Mitochondria have also many other roles including production of various compounds, which will be important later in our story.

Once an independent bacterium, the ancestor of mitochondria somehow found itself inside another cell, survived against all odds, and developed a relationship of interdependence with its new host. Importantly, this interaction added a new trick to the repertoire of our ancestors: the above-mentioned unprecedentedly efficient way of producing energy which enabled an explosion of new, more complex and diverse life forms. To better understand this evolutionary process, scientists were searching for a missing link: a eukaryote lacking mitochondria. The search came up empty. All hot candidates, mostly parasitic protists, were shown to possess a simplified mitochondrion. By studying their mitochondria, researchers found out that no matter how small and simplified the organelle is, it always retains one function: the synthesis of iron-sulfur clusters. These inorganic compounds are essential components of many vital proteins and no cell can live without them. More and more examples accumulated over time supporting two textbook truths: first, there are no ancient amitochondriate eukaryotes living today and second, eukaryotes can never completely lose mitochondria, particularly because they need the iron-sulfur clusters that mitochondria produce.

This is where our work comes in. Among all those false alarms of seemingly amitochondriate protists, one candidate group remained unexplored: Oxymonads. These anaerobic protists are largely neglected as they cause no health issues and have no economic potential whatsoever. Most oxymonads live in the gut of termites, while others, like our research subject Monocercomonoides, inhabit a wider range of hosts - we isolated our specimen from feces of a chinchilla. To date, nothing in the oxymonad cell has been found that resembles a mitochondrion although it is clear that their ancestors must have had one because it is present in their closest free-living relatives. We decided to investigate this case further. By using various experimental methods, we searched for traces of mitochondria and failed. Not only the physical organelle seemed to be missing but also all the proteins that are usually associated with it.

To be absolutely sure, we sequenced all the genetic material of Monocercomonoides in a futile search for a trace of mitochondria. We found everything we would expect from such an organism, but all the mitochondrion-associated genes were missing, including the genes for producing the iron-sulfur clusters. Could Monocercomonoides survive without these molecules? Not so fast! This creature had a surprise for us: a completely different kind of iron-sulfur cluster production system, apparently recently borrowed from bacteria by a process called horizontal gene transfer. So Monocercomonoides freed themselves from their dependence on mitochondria by finding a new way to produce the essential iron sulfur clusters on their own. This is the first report of a eukaryote that completely lost its mitochondria.

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