Proto-eukaryotes and LUCA
I've discussed several "Ur's": Urbilaterians, Ureumetazoans, and Urmetazoans, But now I'm going to go even further back, to the beginnings of the Eukaryotes (nucleated cells), and all life as we know it. Although the hypothetical ancestors don't have names including the "Ur" prefix, they might as well.
The ancestors of the eukaryotes are, in my reconstruction, called the "proto-eukaryotes". This is because I'm assuming that they were pretty much like modern eukaryotes except they lacked mitochondria. One branch of this lineage acquired an endosymbiont, becoming the ancestor of all modern eukaryotes. This is not the only hypothesis for the beginnings of the eukaryotes, the more popular one today is that a fusion of several prokaryotes resulted in modern eukaryotes in a sort of "big bang" process.
The other ancestors, of all life as we know it (except for a few viruses, perhaps), are the Last Universal Common Ancestors (LUCA). Again, my own preference is different from the most common: my preferred reconstruction is for something a lot more like a eukaryote than a "prokaryote", while the most commonly accepted theory is that early protein-using life was very bacteria-like. I'm not unique in my preference, there are also experts who favor this theory:2
Life was born complex and the LUCA displayed that heritage. It had the "body "of a mesophilic eukaryote well before maturing by endosymbiosis into an organism adapted to an atmosphere rich in oxygen. Abundant indications suggest reductive evolution of this complex and heterogeneous entity towards the "prokaryotic" Domains Archaea and Bacteria. The word "prokaryote" should be abandoned because epistemologically unsound.
Phagocytosis and Eukaryogenesis
The paper I'm going to tie this discussion to is by Natalya Yutin, Maxim Y Wolf, Yuri I Wolf, and Eugene V Koonin: The origins of phagocytosis and eukaryogenesis. Its basic thrust is to examine the process of phagocytosis, especially through phylogenetic analysis of the various protein involved in the process, looking for its origins.
Yutin, N., Wolf, M., Wolf, Y., & Koonin, E. (2009). The origins of phagocytosis and eukaryogenesis Biology Direct, 4 (1) DOI: 10.1186/1745-6150-4-9
Figure 1: Phagosomes containing bacteria consumed by phagocytosis. Click on picture to see original.(From Reference 4.)
My biggest problem with this paper is that it carries the built-in assumption that the proto-eukaryotes evolved from a simpler, "prokaryote" (bacteria-like) ancestor. That doesn't invalidate their research, which shows strong relationships between the eukaryotes and the Archaea, the third of the three most deeply divided groups of life as we know it.
The notion that the LUCA possessed a much greater anatomical complexity than modern "prokaryotes" involves several alternatives to the idea that evolution is "always" from simple to complex. The idea that both "simple" lineages (eubacteria and archaea) have become that way through evolutionary simplification is hardly implausible: many species have adopted simplified structures when their lifestyles supported them.
Many analyses have found the actual root of life as we know it to be either between the eubacteria and a clade comprising the archaea and the eukaryotes,8 or somewhere in the eubacteria.13 That makes sense if the LUCA had a simple body, but it makes just as much sense if the LUCA had a fairly complex body and much of its early adaptive radiation took place among creatures with such bodies. Only later, when the oportunities arose, did some branches of the lineages leading to the archaea and the eubacteria become simplified.
In my view, when the world became full of oxygen, and the modern eukaryotes arose through endosymbiosis of the eubacteria that would become mitochondria, all the other lineages with complex bodies were driven to extinction through competition, and only a handful or so of lineages with very reduced bodies survived.
Now, let's return to the subject of the paper here, origins through phagocytosis. This paper1 demonstrates the similarities between the actin proteins used by eukaryotes in phagocytosis, and those possessed by the archaea, putative relatives to the eukaryotes compared to the eubacteria. Others have demonstrated this as well.3, 7
A great deal of the phagocytosis system appears to be poorly conserved, suggesting that the most important parts of it have evolved since the acquisition of mitochondria. It's also likely that the proto-eukaryote was unable to use the fast-growing forms of actin, depending instead on a slower system:1
The branched-filament cytoskeleton allowed the hypothetical [...] ancestor of eukaryotes to produce actin-supported membrane protrusions, resembling eukaryotic lamellipodia/filopodia, thus facilitating occasional engulfment of bacteria. One of such occasions would eventually lead to the mitochondrial endosymbiosis. Conceptually, this process can be regarded as the simplest, primordial form of phagocytosis.
This makes a lot of sense, given that prior to this engulfing the proto-eukaryote would not have had the high-energy system of the mitochondria to power high-speed engulfment of prey, and a slower system would probably have served. After mitochondria, an explosive adaptive radiation would have produced the early divisions of the eukaryotes, with separate refinements of the phagocytosis system, consistent with the demonstration that "[c]omparisons of the complements of proteins that are associated with phagosomes or otherwise implicated in phagocytosis in different eukaryotes show a high level of diversity, with very few components being conserved throughout the eukaryotic domain of life."1
We are left, then, with the picture of a rather slow-moving amoeboid, capable of engulfing immobile prey and detritus, that engulfed and retained a eubacterial endosymbiont.
Origins of the Proto_eukaryotes
What of the origins of this proto-eukaryote? The LUCA probably had some sort of actin-based skeleton, helping to maintain an outer shell of glycoproteins. The eubacteria have something a little like this,7 as do some archaea. The LUCA, then, may well have had a rigid outer cell wall (like many eubacteria and archaea), but may also have had extensions of its plasma membrane into the interior, ancestral to the endoplasmic reticulum.
An interesting theory regarding the origin of the proto-eukaryotes is that they're a fusion of a tubulin-based cell with a nucleus similar to the modern sort, and an actin-based cell with a very flexible and "intelligent" plasma membrane.12 I'm not sure about this, certainly homologues of both tubulin and actin have been found in eubacteria.2, 3, 7
If such a fusion took place, then, it probably did so prior to the division into the the three most basic division of life: eubacteria, archaea, and eukaryotes. I don't regard this as implausible, if we assume that the LUCA was much more like a proto-eukaryote than a "prokaryote" in anatomical complexity.
There are two points to consider here. The first involves the difference between proteins and RNA when it comes to supporting the metabolism catalytically. Both can evidently produce the necessary molecular configuration in solution, but proteins are inherently far better at working across membranes than RNA molecules. This is because RNA possesses no inherently hydrophobic portions while many amino acid residues contain strongly hydrophobic side-groups. (The bases in RNA are partial exceptions to this, but they are normally paired and stacked in helices, and thus unable to face outwards towards the hydrophobic part of the bilipid layer.)
Of course, it's certainly possible to attach hydrophobic molecules to various spots on the RNA molecules, but that's not nearly as effective (IMO) as the inherent ability of proteins to expose large hydrophobic surfaces, especially when coiled in an alpha helix.
What RNA molecules are probably just as good as, if not better, is making "motors". Such ribozymes could well have been shipping vesicles around the cell long before proteins were invented. They could also have been manipulating membranes: attaching a big lipid to an RNA molecule is a great way to "pin" it to a biomembrane. Thus, in my view, it's a lot more plausible that the pre-protein cell depended on a topologically complex internal membrane structure than trans-membrane processes.
The second point has to do with molecules such as tubulin and actin, that are stacked and unstacked like Lego® blocks
Figure 2. Lego® blocks. (From Wiki)
It's certainly possible that, before proteins, such molecules were made of RNA. I suspect, however, that the inherent implausibility of this idea is one reason researchers prefer a "bacterial" model for the earliest inventors of proteins. But there's another possibility when you consider the idea that the LUCA and its immediate ancestors were more like eukaryotes. My suggestion is that the functions now filled by these molecules were once filled by large polysaccharides. These are presently added to proteins in the endoplasmic reticulum (ER) and the Golgi apparatus. The additions include sugars with carboxylate groups, amino groups, and both. Not only that, but the construction process naturally involves multiple branching, unlike proteins, which require special provisions to get branching chains. This means that such polysaccharides have the ability to form complex surfaces with both positive and negative charges on, just as proteins do. If the LUCA and its pre-protein ancestors possessed structures homologous to the ER and Golgi apparatus, they could have manufactured complex sugars that would have served similar purposes to actin and tubulin. Of course, it's actually the other way around: the originals of actin and tubulin evolved as proteins to take the place of the previously used complex sugars.
Complex sugars are still used for structural purposes in many eubacteria, and if the LUCA's ancestry began with such sugars being used for structure, it makes sense that the splitting of basal lineages took place while those sugars were being replaced by proteins. It also makes sense that the various molecular motors that "ride" the cytoskeletal components were originally ribozymes, being replaced by enzymes during the original adaptive radiation of protein-using life.
A point to consider is that the energy cost of hooking two sugars together by their hydroxyl groups is generally less than that of hooking an amino group to a carboxylate, as happens in making proteins. Of course, that begs the question of why proteins replaced complex sugars, but the answer probably has to do with the ease of disassembling these molecules to reuse the amino acids.
Evolution and Complexity
These two points, in my view, add considerable plausibility to the idea that the LUCA was topologically complex.2 In fact, the only real objection remaining to this idea is the prejudice that evolution always has to go from "simple" to "complex".
In the first place, this simply isn't true, as the many documented cases of simplification in evolution attest. In the second place, if there actually was a movement from anatomical simplicity to complexity, it could just as easily have taken place prior to the invention of proteins.
Another point is that "simplicity" is relative. The relative lack of separate compartements in prokaryotes means that all the enzymes have to work in the same "sandbox", which in turn means that they have to "play nicely" with one another. Side reactions of one process that tend to poison another can't be allowed, which considerably reduces the potential for mutation to create new processes. In eukaryotes, as well as proto-eukaryotes, the large number of different cellular compartments specialized for different functions means that new enzymes will often have a much smaller number of other reactions they have to "play nicely" with. This means that the evolutionary process leading to new metabolic reactions is "simpler" chemically for eukaryotes than for prokaryotes.
In fact, I'm personally convinced that the "simple" prokaryotes all began as "stripped down code thieves", stealing DNA sequences from their more topologically complex relatives after those relatives had gone through the process of evolving them. Some of the archaea may have stolen from their proto-eukaryote relatives, while others may have evolved a broadened ability to steal from anybody. As for the Eubacteria, I suspect they stole most of the photosynthetic system from more complex relatives, while also evolving the ability to steal from the eukaryotes. This makes more sense to me than the idea that the eubacteria, in their "stripped down" state, were able to evolve the complex mechanisms of photosynthesis, or even the electron transport system.
Finally, a great deal of work in complexity theory has demonstrated that there's no inherent need to have life to have complexity.16 How life arose is a very contentious question, and while the "RNA World" is the current fad, it's hardly completely accepted.2, 15 I don't really like any of the current theories, but that's a subject for another post (and not the next one).
links: (These aren't all called out in the text. Click the back key to return if you got here via a footnote.)
1. The origins of phagocytosis and eukaryogenesis
2. the last universal common ancestor: emergence, constitution and genetic legacy of an elusive forerunner
3. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa
4. The Phagosome: Compartment with a License to Kill
5. The many faces of actin: matching assembly factors with cellular structures
6. Arp2/3 complex interactions and actin network turnover in lamellipodia
7. The Bacterial Cytoskeleton
8. The Deep Archaeal Roots of Eukaryotes
9. Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode
10. Components of Coated Vesicles and Nuclear Pore Complexes Share a Common Molecular Architecture
11. Rooting the tree of life by transition analyses
12. Eukaryotic Cells and their Cell Bodies: Cell Theory Revised Reference thanks to evolvingideas.
13. Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world
14. Phylogeny of endocytic components yields insight into the process of nonendosymbiotic organelle evolution
15. On the Chemistry and Evolution of the Pioneer Organism
16. The Origins of Order: Self-Organization and Selection in Evolution by Stuart A. Kauffman