An unseen organism and a hypothesis about the origin of viruses

What is a parasite? A definition that often comes up is this one:

Parasites, in a phrase, are predators that eat prey in units of less than one.

Edward O. Wilson, The Meaning of Human Existence (2014)

The sentence is funny, but in my opinion it’s not really a good definition.

First, what about “units of less than one”? Terrestrial herbivores often eat only a few leaves from a plant; in the ocean, cookiecutter sharks literally “eat prey in units of less than one”. Yet, I wouldn’t consider them parasites. In the microbial world where individuals are single cells, it is difficult for parasites to chew off “less than one” prey. Syndiniales (dinoflagellate parasites of other dinoflagellates), when they infect a host cell, exploit the entirety of the cell, multiply inside it and eventually kill it by bursting out, alien-style. Should we consider them as predators then?

Rather than units of prey, there’s a temporal aspect that can separate predation and parasitism: while the first is a one-time encounter, the second implies prolonged contact¹. In that sense, parasitism is a form of symbiosis (from the greek: “living with”).

Second, parasitism doesn’t necessarily involve a prey-predator relationship. Cuckoos are considered parasitic birds, because they lay their eggs in the nests of gullible victims that will raise their offspring and bear the cost of parental duties².

So, let’s propose another definition: a parasite is an organism that offloads some of its “work” to another organism it lives with, without providing a service in return. In the most extreme case, this can mean “breaking into your cytoplasm and exploiting YOUR cellular machinery to produce MY organic matter until you die”, as in the modus operandi of syndiniales. Or it can be more insidious.

The frontier between mutualistic symbiosis and parasitism is blurry. In a 2-partner symbiosis, each partner is incentivised to give as little as possible to the other, while taking the maximum³. A crafty cheater will manage to transform a mutualistic interaction into a parasitic relationship. As Husnik et al. (2021) eloquently write:

Overall, there is a growing body of evidence suggesting that discrete categories of fitness-defined symbioses, like parasitism and mutualism, may only really be informative for the most extreme ends of the spectrum, and that symbioses should be rather viewed as ongoing and context-dependent power struggles.

Filip Husnik et al. “Bacterial and archaeal symbioses with protists”, Current Biology (2021) https://doi.org/10.1016/j.cub.2021.05.049

At the cellular level, “offloading work” means abandoning some essential functions (for instance, the ability to import specific nutrients or synthesise key metabolites) and letting a partner cell provide it for you. The goal is to let your partner do as much as possible while you live off the resources it provides. How far can such a lifestyle lead you?

The microbiome of microbes

The concept of microbiome is now fairly well-known outside of biology’s inner circles, mostly thanks to the rising fame of the human gut microbiome. It refers to an ensemble of microbes that live in close association with a host. By many aspects, it forms an ecosystem in its own right, shaped in great part by the peculiar environment it inhabits (for instance, the human gut is characterised by total darkness, a temperature precisely set to 37°C and the periodic arrival of large quantities of nutritious matter, i.e., food.)

What’s funny is that many microbes harbour their very own microbiome. Protists are generally much much larger than prokaryotes, so they too live in close association with a variety of small tenants. In the case of microalgae, this micro-microbiome is called the phycosphere, and is located within the viscous layer in the direct vicinity of the cell.

In some cases, specific phycosphere bacteria take a preeminent role in the lifestyle of their host, so much so that the two partners are considered to form a symbiosis.

This is the dinoflagellate Citharistes regius. It looks like a Dinophysis (they belong to the same family), but with a sort of kangaroo pouch where it keeps its bright orange symbiotic cyanobacteria, or cyanobionts. The dinoflagellate itself is not photosynthetic (it lacks chloroplasts) so it relies on its personal photosynthetic garden. The cyanobionts, hidden in the pouch, are somewhat protected from the vicissitudes of a solitary planktonic life.

No wonder some planktologists would want to investigate this eccentric duo. That’s why researchers in Japan picked one cell of C. regius they found in their backyard⁴, and sequenced all the prokaryotic genomes inside it. It turned out that the most interesting part of C. regius‘ microbiome weren’t the cyanobionts, but an unexpected hitchhiker. They detailed their discovery in a great preprint they published last year, that I will now discuss.

An unusually minimalist genome

After they assembled the sequenced fragments, they ended up with 5 circular, continuous DNA sequences:

• Expectedly, the chromosome of the symbiotic cyanobacteria, along what looked to be a plasmid (a very small circular sequence of DNA that replicates independently of the chromosomal genome in bacteria).
• The genomes of 2 gammaproteobacteria, likely intracellular parasites.
• And, most surprisingly, the weird, minuscule, but apparently complete genome of an archaeon.

The archaeal genome in question was only 238 thousands of base pairs, with 222 genes coding for 189 proteins (and 33 essential RNAs). Such a small size immediately places it among the smallest prokaryotic genomes, and well below many viral genomes (see the figure in this post for instance). To give you an idea, the first completely sequenced genome of Escherichia coli (respectable for a prokaryote, but by no means a giant) was 4.6 million base pairs long, with a grand total of 4288 protein-coding genes.

The discoverers of this mysterious archaeon decided it deserved a proper name: Candidatus⁵ Sukunaarchaeum mirabile. The genus name comes from Sukuna-biko-na, a japanese deity known for his very small size⁶; mirabile means “extraordinary” or “miraculous”, because of the enigma its tiny genome represents.

Life and times of Sukunaarchaeum

What does such an organism do? What does it even look like? One way to get an idea is to look at which genes are present in its genome; and which ones are absent.

Almost all the annotated genes (i.e., those for which a known function is known or suspected) in S. mirabile‘s genome are dedicated to transcription, translation and protein management. The number of genes dedicated to metabolism is exceptionally low, even compared to other parasitic prokaryotes, with exactly zero genes dedicated to lipid, nucleotide or amino acid metabolism.

What this means in essence is that the only functions coded by the Sukunaarchaeum genome are dedicated to replicating it. Or, more exactly, to replicating it and assembling 8 very large proteins with several transmembrane helices which indicate that they are likely located at the cell membrane. This leads Harada et al. to propose this police sketch of Sukunaarchaeum:

To survive without any cellular machinery dedicated to metabolism, S. mirabile likely lives inside C. regius, mooching off its host. This is certainly implied by the fact it was found in a cell of this dinoflagellate, but n=1 is too few observations to draw sweeping conclusions. To confirm the association between host and parasite, the authors pulled an elegant analysis of some publically available data.

Tara Oceans is a scientific program and expedition that aims at taking a global census of planktonic life in Earth’s oceans. To probe the ocean’s biodiversity, the scientists onbard Tara filter large volumes of seawater at sampling stations all around the world, and then sequence all the DNA that is trapped on the filter. By identifying the organisms with a specific DNA sequence (called a barcode), they can know the organisms present in the sample. What’s great is that all the barcodes belonging to unknown organisms are also recorded, so scientists can come back years later to see if their newly discovered organism was present here or there. That’s exactly what Harada et al. did.

This figure requires some explanations. In a, you can see a phylogenetic tree of archaeal barcodes in the whole Tara Oceans dataset. It turns out that the Sukunaarchaeum mirabile the authors found off the coast of Japan is not alone, and that there is an entire family of related archaea, that they call the “Sukuna-clade”.

Onboard Tara, the water is filtered on different sieves, to separate planktonic organisms according to their size. In b, the heatmap shows the proportion of barcodes belonging to several members of the Sukuna-clade detected in 3 size fractions : 0.5-5 µm, 5-20 µm and 20-180 µm. We see that the Sukuna-clade archaea are mainly present in the 5-20 µm fraction (orange = higher proportion). Because archaea are generally smaller, finding them in this fraction indicates that they are likely associated with bigger host cells⁷.

Finally, in c we can see that the highest proportion of Sukuna-clade barcodes is found in the sampling station (Tara 76) that also has the highest proportion of barcodes for the Dinophysiales, the family of dinoflagellates Citharistes regius belongs to.

(d is just a phylogenetic tree showing the position of the original Sukunaarchaeum mirabile genome in the “Sukuna-clade”. It’s not really important.)

The ultimate parasite

Let’s recap. There’s a whole family of archaea that live in the plankton, in close association with dinoflagellates of the Dinophysiales family. The genome of one of these archaea, Sukunaarchaeum mirabile, found inside the dinoflagellate Citharistes regius, is among the smallest prokaryotic genomes known to date, if not the smallest. Said genome seems almost entirely dedicated to self-replication.

So, it seems that S. mirabile and its family have relinquished any metabolic ambition they once had to focus only on replication. Maybe, in some distant past, their ancestors were useful to their dinoflagellate partner by providing some essential compound, who knows. But, in the comfortable environment of the host cell, with food coming in regularly, they lost 1 metabolic function, then 2, then 3… Like cellular equivalents of Spiegelman’s monsters, they shrank to the smallest entity capable of replication, living entirely at the expense of their host. The parasite’s dream come true.

Sukunaarchaeum is a cell that seems to have a viral-like lifestyle. The only difference between it and a virus is that it retains the machinery responsible for transcription, translation and protein synthesis. But it’s just one step away from becoming a proper virus. Admittedly, it’s still a very big step. Nevertheless, this may consitute a clue about a possible origin of viruses: parasites that succeeded beyond all expectations.

Some thoughts on molecular biology

To finish this post, I’d like to highlight something I find remarkable in this story: the organism at the center of this preprint, that help us draw grand hypotheses about biology and evolution, has never been observed.

When my colleague Rossana taught me RNA extraction, I spent hours squinting at small tubes with translucent RNA pellets that I really needed to not discard with the equally translucent supernatant. Out of frustration (and, I must say, in admiration of her ability to do that effortlessly), I told her that molecular biology was “the science of nothing”.

I should probably change my clever formula to “the science of the invisible”. Because, albeit almost impossible to observe, these molecules are a window into an invisible universe of processes, origins and interactions. And this surely is “something”.

This blog post is based on the preprint by Ryo Harada et al. “A cellular entity retaining only its replicative core: Hidden archaeal lineage with an ultra-reduced genome” published on biorXiv in May 2025. https://doi.org/10.1101/2025.05.02.651781

I really thank the authors for making this fascinating piece of work public, and under a CC BY licence so we can discuss it openly.

The authors also published peer-reviewed papers on the cyanobacteria (https://doi.org/10.1038/s41598-024-63502-0) and the 2 gammaproteobacteria (https://doi.org/10.1264/jsme2.ME25005) they found within the Citharistes regius cell, that are interesting too.

This entire blog post is under a CC BY 4.0 license, you can reuse parts of it as long as you cite the original author(s) properly.

(I also thank 2 “anonymous” reviewers, who will recognise themselves, for their helpful comments.)

1. Of course, what registers as prolonged contact depends of the lifespan of the organisms considered. A few hours may appear short for mammals, but in the microbial world it could very well be considered a prolonged contact. ↩︎
2. Although, because life is a merciless arms race, the victims are not so gullible and will ruthlessly cull any detected intruder. ↩︎
3. To a friend of mine who asked me how it was like sharing a flat with my brother, I once jokingly sent a paragraph from a paper on a planktonic symbiosis wondering if it was “Mutualism or Enslavement?”
   (Bro, if you’re reading this, it was only a joke! Living with you was a fun time.) ↩︎
4. Well, they found it in the sea not too far from their lab, which is a marine biologist’s equivalent of a backyard. ↩︎
5. According to the rules of prokaryote taxonomy, to officially give a name to an organism, one needs to first establish a culture of it. If you want to name a wild prokaryote that you haven’t successfully cultivated yet, you can add the title Candidatus (“candidate” in latin, abbreviated Ca.) to the proposed name. ↩︎
6. There’s apparently a tradition among microbiologists to name archaea with a reference to deities. There’s even a clade known as the Asgard archaea (after the home of Nordic gods), with all the expected Ca. Lokiarchaeum, Ca. Freyarchaeum, Ca. Heimdallarchaeum etc. ↩︎
7. This is not the first time these authors pull this elegant trick with the Tara Oceans size fractions, they already did it in a fantastic paper on Ornithocercus, another dinoflagellate in symbiosis with cyanobacteria. There’s definitely something with Japanese marine biologists and creative studies involving serial filtration of plankton. ↩︎