Eukaryote Missing Link?

[lpetrich]

One of the first things that one learns when one studies microbiology is the difference between prokaryotic and eukaryotic cells. Eukaryotic ones have much more internal complexity than prokaryotic ones, lots more "organelles".

Some of this complexity is known to be the result of endosymbiosis, mitochondria being descended from some alpha-proteobacterium, and chloroplasts from some cyanobacterium.

But the rest of the cell is much more mysterious. Prokaryotes are divided into two domains, Bacteria (or Eubacteria) and Archaea, and the eukaryotic cell's information systems are most closely related to archaeal ones. So was the ancestral eukaryote some archaeon that liked to eat other microbes? Many eukaryotes continue to do this, something called phagocytosis. This would also explain endosymbiosis.

But recently, an organism has been discovered that seems to be an Archaea - Eukarya "missing link". It was discovered by sequencing the genes of organisms found in deep-ocean mud, and doing so without bothering to sort them out. Metagenomics, as it's called, has become a popular way of sampling communities of microbes.

The Third Domain: Lokiarchaeota - The shapeshifter bug in the mud

One thing that is interesting with eukaryotes is that they look a bit like archaea and a bit like bacteria (and a lot like none of them). And here is what's really interesting with Lokiarchaea. They have DNA that is shared with many other archaea, but they also have DNA normally found only in eukaryotes. In fact, they are more closely related to eukaryotes than any other archaea that we have ever seen before.

The Lokiarchaea have pieces of DNA - genes - that codes for actin. That is a protein that was previously only known from eukaryotes and is used for all sort of things that relates to the cell shape. It can be used to bend and form the cell. It can be used to send signal from one part to the other - and it can be used to pick up things from outside the cell.

New Loki Microbe is Closest Relative to All Complex Life – Phenomena: Not Exactly Rocket Science

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.

Newly found microbe is close relative of complex life - BBC News
Its discoverers plan to search in places like Yellowstone Park, with its hot springs.

Complex archaea that bridge the gap between prokaryotes and eukaryotes (journal article)

It has been known for some time that several members of the TACK superphylum of Archaea have some genes for "eukaryotic signature proteins", proteins typical of eukaryotes and seldom found elsewhere. These include actin and tubulin, proteins involved in the eukaryote cytoskeleton, proteins involved in moving parts of the cell around, and also in changing the cell's shape. Also some cell-division proteins related to some proteins involved in material transport in a eukaryotic cell.

Then some ocean-floor metagenome explorers found genetic evidence of an organism that they named Lokiarchaeum. It turned out to be an early-branching member of TACK (Thaumarchaeota, Aigarchaeota, Crenarchaeota, Korarchaeota), and its discoverers have proposed a phylum for it, Lokiarchaeota.

Most notably, a significant part of the predicted proteome (175 proteins or 3.3%) was most similar to eukaryotic proteins (Fig. 2c) and revealed a dominance of proteins, which in eukaryotes are involved in membrane deformation and cell shape formation processes, including phagocytosis (37) (Extended Data Table 1 and Supplementary Table 6).

Contamination from eukaryotes?

The authors examined are confident that it is not the case. The genes for these proteins are surrounded by more typical Archaea genes, the genes are outside the family trees of their eukaryotic counterparts, and the organism has a typical archaeal-style informational system.

Actins represent key structural proteins of eukaryotic cells and comprise filaments that are crucial for various cellular processes, including cell division, motility, vesicle trafficking and phagocytosis (39). The Lokiarchaeum genome encodes five actin homologues that display higher similarity to eukaryotic actins and actin-related proteins (ARPs) than to crenactins, a group of archaeal actin homologues that were recently shown to be involved in cell shape formation (25,37,40) (Supplementary Table 6).

Lokiarchaeum also has a lot of Ras-family small GTPases, a family of proteins very common in eukaryotes but rare elsewhere. These are involved in regulation of a variety of cell processes, including shaping and material transport.

It also has another set of eukaryote proteins, those involved in the ESCRT cellular machinery. It is involved in degradation of unwanted proteins and material transport and budding processes.

"It is also noteworthy that Lokiarchaeum appears to encode the most ‘eukaryotic-like’ ribosome identified in Archaea thus far."

Taken together, our data indicate that the archaeal ancestor of eukaryotes was even more complex than previously inferred (2) and allow us to speculate on the timing and order of several key events in the process of eukaryogenesis. For example, the identification of archaeal genes involved in membrane remodelling and vesicular trafficking processes indicates that the emergence of cellular complexity was already underway before the acquisition of the mitochondrial endosymbiont, which now appears to be a universal feature of all eukaryotes (28,37,50). Indeed, based upon our results it seems plausible that the archaeal ancestor of eukaryotes had a dynamic actin cytoskeleton and potentially endo- and/or phagocytic capabilities, which would have facilitated the invagination of the mitochondrial progenitor.

The authors propose that the ancestor of TACK had already had this complicated cellular machinery, but that the ancestors of many of TACK's branches later lost much of it.

 

[lpetrich]

Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier?
From the abstract, expanded:

First, evolutionary reconstructions suggest complex ancestors for most of the major groups of archaea, with the subsequent evolution dominated by gene loss.

Second, homologues of signature eukaryotic proteins, such as actin and tubulin that form the core of the cytoskeleton or the ubiquitin system, have been detected in diverse archaea. The discovery of this ‘dispersed eukaryome’ implies that the archaeal ancestor of eukaryotes was a complex cell that might have been capable of a primitive form of phagocytosis and thus conducive to endosymbiont capture.

Third, phylogenomic analyses converge on the origin of most eukaryotic genes of archaeal descent from within the archaeal evolutionary tree, specifically, the TACK superphylum.

Fourth, evidence has been presented that the origin of the major archaeal phyla involved massive acquisition of bacterial genes. Taken together, these findings make the symbiogenetic scenario for the origin of eukaryotes considerably more plausible and the origin of the organizational complexity of eukaryotic cells more readily explainable than they appeared until recently.

He has an addendum:

Shortly after this manuscript was submitted, a game-changing discovery bearing on the archaeal ancestry of eukaryotes has been published [161,162]. Deep metagenomic sequencing uncovered a remarkable group of archaea from marine sludge that combined the two key properties expected of the eukaryotic ancestor. First, one of these novel organisms, tentatively classified as a new phylum Lokiarchaeota (already affectionately known as Loki), represents a sister group to eukaryotes, and the Loki–eukaryote branch is confidently lodged deep within the TACK superphylum. Second, the genome of Loki recapitulates with an uncanny precision the reconstructed gene repertoire of the putative archaeal ancestor of eukaryotes that is outlined above. In particular, Loki encode crenactins, homologues of eukaryotic gelsolins, the ESCRT-III complex, an expanded family of small Ras-like GTPases and the complete ubiquitin system. This gene repertoire translates into a confident prediction of a complex cytoskeleton and membrane remodelling systems and is compatible with a rudimentary phagocytic capability that has been predicted for the archaeal ancestor of eukaryotes. Further exploration of the genomes and hopefully the actual biology of the Loki are likely to dramatically enhance our understanding of eukaryogenesis

The Eukaryotic Ancestor Had a Complex Ubiquitin Signaling System of Archaeal Origin
From its abstract:

We found that the Ub toolkit had a pre-eukaryotic origin and is present in three extant archaeal groups. The pre-eukaryotic Ub toolkit greatly expanded during eukaryogenesis, through massive gene innovation and diversification of protein domain architectures. This resulted in a LECA with essentially all of the Ub-related genes, including the SUMO and Ufm1 Ub-like systems. Ub and SUMO signaling further expanded during eukaryotic evolution, especially labeling and delabeling enzymes responsible for substrate selection.

So some early archaeon had it, and it became expanded in the ancestral eukaryote and also in later eukaryotes.

Endosymbiotic origin and differential loss of eukaryotic genes : Nature : Nature Publishing Group
From its abstract, expanded:

Our results indicate

(1) that gene transfer from bacteria to eukaryotes is episodic, as revealed by gene distributions, and coincides with major evolutionary transitions at the origin of chloroplasts and mitochondria;

(2) that gene inheritance in eukaryotes is vertical, as revealed by extensive topological comparison, sparse gene distributions stemming from differential loss; and

(3) that continuous, lineage-specific lateral gene transfer, although it sometimes occurs, does not contribute to long-term gene content evolution in eukaryotic genomes.

That is, eukaryotes don't do much horizontal gene transfer, unlike prokaryotes.

Eukaryote sex is ancestral and widespread -- It does not seem to have much by way of prokaryotic antecedents, even though it's almost certainly ancestral. The eukaryotic endomembrane system (nuclear membrane, endoplasmic reticulum, Golgi apparatus) also has an obscure origin.

Archaeal histones: structures, stability and DNA binding. - PubMed - NCBI -- much like eukaryotic ones. In eukaryotes, histones are proteins that bind DNA into structures called nucleosomes.

Archaeal nucleosomes -- some archaea also have this eukaryotic structure.


So a lot of distinctive features of eukaryotes are not quite distinctive, but instead, evolved in ancestors in Archaea.