New Loki Microbe is Closest Relative to All Complex Life

Loki’s Castle lies midway between Greenland and Norway, around 2,300 metres below the ocean surface. It’s a field of hydrothermal vents—black, rocky chimneys that belch out volcanically superheated water. And yet, despite the hellish landscape, life abounds here.

Now, fifteen kilometres away from the vents, a team of scientists led by Thijs Ettema from Uppsala University have discovered a new group of very special microbes. They are the closest living relatives of all eukaryotes—the huge group that includes every animal, plant, fungus, and all other complex life on the planet.

Ettema named his new microbes the Lokiarchaeota (low-key-ar-kay-oh-tuh), partly after the vents where they were found but also partly after the Norse deity whom the vents were named after. Loki was a trickster and a shape-shifter. As Ettema writes, he has been described as “a staggeringly complex, confusing, and ambivalent figure who has been the catalyst of countless unresolved scholarly controversies”. The same could be said about the eukaryotes themselves.

The eukaryotes include all the organisms that we’re most familiar with, and certainly all the ones we can see with our naked eyes. But they are just one of three grand groups, or domains, to which every living thing belongs. The other two—bacteria and archaea—both consist of single cells. They look superficially similar but biochemically, they are worlds apart.

The bacteria and archaea (collectively known as prokaryotes) are masters of biochemistry. They can survive in extreme conditions and eat everything from crude oil to metal. But for all their tricks, they are incredibly simple when compared to eukaryotes. Our cells contain internal compartments, like a nucleus that packages DNA and mitochondria that provide us with energy; bacteria have none of that. Our cells have a complex internal skeleton that provides structural support and shuttles molecules around; bacteria do not. Our genomes are much bigger than theirs.

So, there’s a huge gulf between prokaryotic cells and eukaryotic ones, and that gulf has only ever been breached once. All eukaryotes descend from a common ancestor that arose just over 2 billion years ago. Bacteria had been around for at least a billion years before that and in all that time, they stayed simple. Some of them have made small forays into eukaryote-ness, picking up one or two complex traits, but none have ever made it all the way, except that one time. Why?

One answer—the one that I prefer—is that the eukaryotes were born through a singularly improbable merger between an archaeon and a bacterium. The bacterium eventually became the mitochondria that exist in all our cells. It provided its archaeon host with an extra source of energy, allowing it to break free of its evolutionary constraints and achieve newfound levels of genetic and physical complexity. (For the full story of this event, and why many scientists believed it played out like this, see my Nautilus piece.)

We know that the ancient bacterium was part of the alphaproteobacteria, a group whose many members still have a habit of finding their way into other cells. But what about the archaeon? Which group did it belong to? Until now, we didn’t know, largely because the archaea are so poorly studied.

To solve this mystery, Ettema’s group scoured ocean floor sediments, which often harbour new archaeal groups. Loki’s Castle was the first place they looked and, amazingly, the Lokiarchaeota were living in the very first sample they analysed.

By sequencing the DNA in the sample, they reconstructed one mostly complete genome (which they called Lokiarchaeum, or just Loki for short) and two partial ones. The team haven’t actually see the archaea themselves; they only know about them through their genome. That’s okay—a lot of microbes were discovered in this genome-first manner, and genes can tell you a lot about what an organism is like. Loki’s genes, for example, hint that it might have features that were thought to be exclusive to eukaryotes.

It has five genes for actins—molecules that eukaryotes use to build their internal cytoskeletons. It has genes that pinch off parts of a cell’s membrane, helping it to divide in two or to package unwanted molecules for recycling. And it has a huge number of genes for supposedly eukaryotic enzymes called small GTPases that, among various jobs, also help to control and remodel a cell’s internal skeleton.

As Ettema writes, “It is tempting to speculate that Lokiarchaeum has a dynamic actin skeleton.” These skeletons don’t just move molecules around; they also allow eukaryotic cells to change their shape and swallow other cells—a process called phagocytosis. Loki’s genome, especially its small GTPases, “is not direct evidence that this group is capable of phagocytosis, but it is a smoking gun,” says James MacInerney from Maynooth University.

“They help us to get around some of the issues we have had before when thinking of eukaryotes as a merger of two prokaryote groups,” he adds. Critics of the merger idea have argued that a bacterium couldn’t possibly get inside an archaeon if neither was capable of swallowing the other (although this does sometimes happen). They’ve also noted that neither group had an extensive cytoskeleton, so where did the eukaryotic one come from? Well, here is an archaeon that has hints of both a cytoskeleton and phagocytosis—or, more likely, primitive precursors of both. “We’ve got a little bit closer to understanding how that complexity evolved,” adds Ettema.

To clarify, Loki is a modern microbe. It is not our ancestor, but it could well be part of the group that our ancestor also belonged to. And it hints that said ancestor was more complex than we thought. “It helps us to see an easier path from being prokaryote to being eukaryote,” says MacInerney. “It looks like the archaebacterial host for the merger that gave rise to eukaryotes could have been a kind of bug that, up to now, some people said would not exist.  It was ready to be a host. It had some key genes that made it a good host.”

Nick Lane from UCL, who has a new book out on the origin of complex life, is less convinced. “The conclusions are overblown,” he says. “[Loki] provides a more interesting view of what archaea can do, which is more than we thought, but it’s 1% of the way to being a eukaryote. They use the phrase “It’s tempting to speculate”, which means “there’s no evidence for”. I’d wager a bet that when anyone dredges one up from the bottom of the ocean, it’ll be 1-2 microns long, it won’t do phagocytosis, and it’ll be a bona fide prokaryote.”

My sense is that Lane and Ettema agree more than they disagree. Ettema doesn’t believe that Loki sits halfway between prokaryotes and eukaryotes; “It just makes the gap a little smaller,” he says. “It’s premature to say that it’s phagocytotic, but it has the ingredients. Maybe it’s on its way to find out how to do this.” And regardless of what exactly Loki was like, it gives credence to the merger idea. It clearly shows that eukaryotes evolved from the archaea, rather than the old model in which the two domains are sister groups. We are essentially archaea, given an evolutionary rocket boost thanks to a bacterial add-on.

Ettema’s priority is now to see Loki in the cellular flesh. “If we could get an image of those cells and how complex they really are, that would tell us a lot. That’s something very high on the priority list,” he says. “This study is based on 10 grams of sediment, and the number of cells is very limited. And for some reason, Loki doesn’t want to get out of the sediment.

They are also going to look for more archaea in more deep sea sediments. Given how quickly they found Loki, it’s likely that they’ll find even more new groups of archaea, some of which will be even more closely related to us.

Reference: Spang, Saw, Jørgensen, Zaremba-Niedzwiedzka, Martijn, Lind, van Eijk, Schleper, Guy & Ettema. 2015. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature http://dx.doi.org/10.1038/nature14447

More on the origin of life, and of eukaryotes:

• The origin of complex life – it was all about energy
• Scientists finish a 53-year-old classic experiment on the origins of life
• The two-genome waltz: how the threat of mismatched partners shapes complex life
• Life’s Rocky Start
• The Unique Merger That Made You (and Ewe, and Yew)