In Depth › Analysis and Opinion

Evolution of complex life on Earth, take 2?

A mysterious cell from the deep defies classification, but it ticks all the boxes for an organism in the process of evolving from bacteria to more complex life, writes Nick Lane.

More than 1,200 metres deep in the Pacific Ocean off the coast of Japan lies an underwater volcano named Myojin Knoll. A team of Japanese biologists have been trawling these waters for more than a decade, searching for interesting life forms.

By their own account, they didn't find anything terribly surprising until May 2010, when they collected some segmented worms clinging to a hydrothermal vent.

It wasn't the worms that were interesting but the microbes associated with them. Well, one of the microbes - one cell that looked a lot like a eukaryote (the kind of complex cell found in all animals, plants, algae and fungi), until they looked at it more closely. Then it became the most teasing enigma.

Eukaryote means 'true nucleus', and this cell (below) has a structure that on first glance looks like a normal nucleus (N). It also has other internal membranes, and some endosymbionts (small symbiotic partners living inside the cell, like mitochondria or chloroplasts, labelled E).

Like eukaryotic fungi and algae, it has a cell wall (CW); and not surprisingly, for a specimen from the deep black ocean, it lacks chloroplasts. The cell is reasonably large, with a volume about 100 times larger than a typical bacterium. The nucleus is large too, taking up nearly half the cell.

On a quick glance, then, this cell isn't easy to classify into a known group, but it is plainly eukaryotic. It's only a matter of time and gene sequencing, you might think, before it is safely assigned to its proper home in the tree of life.

Oh, but look again! All eukaryotes have a nucleus, true, but in all known cases that nucleus is similar in its structure. It has a doubled membrane, continuous with other cellular membranes. The DNA is carefully packaged into relatively thick chromosomes, and the cell's proteins are synthesised on ribosomes that are always excluded from the nucleus. This is the very basis of the distinction between the nucleus and cytoplasm.

So what about the cell from Myojin Knoll? It has a single nuclear membrane, with a few gaps. No nuclear pores. The DNA is composed of fine fibres as in bacteria, not thick eukaryotic chromosomes. There are ribosomes in the nucleus. Ribosomes in the nucleus! And ribosomes outside the nucleus too. The nuclear membrane is continuous with the cell membrane in several places. And some of the endosymbionts have a resemble corkscrew shaped bacteria on 3D reconstruction, making them look more like relatively recent bacterial acquisitions.

While it has internal membranes there is nothing resembling an endoplasmic reticulum, or the Golgi apparatus, or a cytoskeleton, all classic eukaryotic traits. In other words, this cell is actually nothing like a modern eukaryote. It just bears a superficial resemblance.

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Prokaryote vs Eukaryote vs …?

So what is it, then? The authors didn't know. They named the beast Parakaryon myojinensis, the new term 'parakaryote' signifying its intermediate morphology. Their paper, published in the Journal of Electron Microscopy, had one of the most tantalising titles I've ever seen: 'Prokaryote or eukaryote? A unique microorganism from the deep sea'

Having set up the question beautifully, the paper goes nowhere at all in answering it. A genome sequence would give some insight into the true identity of the cell, and turn this largely overlooked scientific footnote into a high-impact Nature paper. But they had sectioned their only sample for microcospy. All they can say for sure is that in 15 years and 10,000 electron microscopy sections, they had never seen anything remotely similar before. They haven't seen anything similar since, either.

The unusual traits could be an artefact of preparation — a possibility that is not to be discounted, given the troubled history of electron microscopy. On the other hand, if the traits are just an artefact, why was this sample a unique oddity? And why do the structures look so reasonable in themselves? I'd hazard it's not an artefact. That leaves three conceivable alternatives.

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A highly adapted eukaryote?

It could be a highly derived eukaryote, which changed its normal structures as it adapted to an unusual lifestyle, clinging to the back of a deep-sea worm on a hydrothermal vent. But that seems unlikely. Plenty of other cells live in similar circumstances, and they have not followed suit.

In general, highly derived eukaryotes lose archetypal eukaryotic traits, but those that remain are still recognisably eukaryotic. That's true of all the archezoa, for example, those purportedly living fossils that were once thought to be primitive intermediates but eventually turned out to be derived from fully fledged eukaryotes.

If Parakaryon myojinensis really is a highly derived eukaryote, then it's radically different in its basic plan to anything we've seen before. I don't think that's what it is.

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A living fossil?

Alternatively, it could be a real living fossil, a 'genuine archezoan' that somehow clung to existence, failing to evolve the modern range of eukaryotic accessories in the unchanging deep oceans.

This explanation is favoured by the authors of the paper, but I don't believe that either. It is not living in an unchanging environment: it is attached to the back of a segmented worm, a complex multicellular eukaryote that obviously did not exist in the early evolution of eukaryotes.

The low population density — just a single cell discovered after many years of trawling — also makes me doubt that it could have survived unchanged for nearly 2 billion years. Small populations are highly prone to extinction. If the population expands, fine; but if not, it's only a matter of time before random statistical chance pushes it into oblivion. Two billion years is a very long time — about 30 times longer than the period coelacanths are thought to have survived as living fossils in the deep oceans. Any genuine survivors from the early days of the eukaryotes would have to be at least as populous as the real archezoa to survive that long.

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Complex life on Earth, take 2

That leaves the final possibility. As Sherlock Holmes remarked, 'When you have eliminated all which is impossible, then whatever remains, however improbable, must be the truth.' While the other two options are by no means impossible, this third is the most interesting: it is a prokaryote, which has acquired endosymbionts, and is changing into a cell that resembles a eukaryote.

If this is indeed the case, Parakaryon myojinensis is undergoing the very step that is necessary for the evolution of complex life - eukaryotes — from prokaryotes: endosymbiosis. Every eukaryote on Earth evolved from a single endosymbiosis between a prokaryote host cell and the bacteria that became mitochondria.

To my mind, this third option makes the most sense. It immediately explains why the population density is low; endosymbioses between prokaryotes are rare and are beset by logistical difficulties.

An endosymbiosis between prokaryotes also explains why this cell has various traits that look eukaryotic, but on closer inspection are not. It is relatively large, with a genome that looks substantially larger than any other prokaryote, housed in a 'nucleus' continuous with internal membranes, and so on. These are all traits that we predict would evolve, from first principles, in prokaryotes with endosymbionts.

If Parakaryon myojinensis is repeating eukaryotic evolution, as I suspect, its extremely low population density (just one specimen in 15 years of hunting) is predictable.

Even if other P myojinensis cells exist in the deep, the most likely fate for the species is extinction. Perhaps it will die because it has not proceeded far enough along the path towards becoming a eukaryote — it hasn't yet excluded all its ribosomes from its nuclear compartment; and it has not yet 'invented ' sex.

Or perhaps — chance in a million — it will succeed, and seed a second coming of eukaryotes on earth. Only time, and trawling, will tell.

About the author: Dr Nick Lane is an evolutionary biochemist at University College London, where he leads the Origins of Life Programme. This is an edited extract from his latest book, The Vital Question: Why is Life the way it is, published by Profile Books. His previous books include the award-winning Life Ascending: The Ten Great Inventions of Evolution.



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