He became famous (infamous?) for challenging the Three Domain Hypothesis of Carl Woese (and friends) and for advocating better methods of constructing gene trees. Jim Lake proposed that eukaryote nuclei arose from within the archaebacterial clade and not as a sister groups of Archaea as the Three Domain Hypothesis claimed. The sister group was the "eocytes," represented at the time by Sulfolobus solfataricus, an archaebacterium that lives in hot springs (~80°C) and uses sulfur as a source of energy.
The title of his paper is simply, "Eukaryotic origins" (Lake, 2015) and it's very fitting that it's the first paper since the current consensus is that he was right all along and the Three Domain Hypothesis is dead. Vindication. Jim Lake is a very modest man (unlike some of the proponent of the Three Domain Hypothesis) so I'm glad to see that he is getting the recognition he deserves.
Here's the abstract of his paper.
The origin of the eukaryotes is a fundamental scientific question that for over 30 years has generated a spirited debate between the competing Archaea (or three domains) tree and the eocyte tree. As eukaryotes ourselves, humans have a personal interest in our origins. Eukaryotes contain their defining organelle, the nucleus, after which they are named. They have a complex evolutionary history, over time acquiring multiple organelles, including mitochondria, chloroplasts, smooth and rough endoplasmic reticula, and other organelles all of which may hint at their origins. It is the evolutionary history of the nucleus and their other organelles that have intrigued molecular evolutionists, myself included, for the past 30 years and which continues to hold our interest as increasingly compelling evidence favours the eocyte tree. As with any orthodoxy, it takes time to embrace new concepts and techniques.
A few years later (1988), Lake published a very famous paper in Nature in which he challenged the ribosomal RNAs trees that were used to promote the Three Domain Hypothesis. Naturally there was lots of criticism from other scientists but there was also criticism from anti-evolutionists and he quotes one of them in the paper ....
"... you say humans came from an organism that lived at high temperatures and smelled of sulfur. I have news for you, that's not where we came from, that's where you're going."Lots of scientists are now talking about a ring of life as opposed to a tree because most of the genes in eukaryotes don't come from the Eocyte branch but from bacteria via endosymbiotes such as those that became mitochondria and chloroplasts. Lake's figure is complex but you get the general idea—two (or more) lineages fuse to form the first eukaryotes.
Lake, J. (2015) Eukaryotic origins. Phil. Tran. R. Soc. B 370: Published online Aug. 31, 2015 [doi: 10.1098/rstb.2014.0321]
75 comments :
A very useful summary! Just one little thing: the correct DOI reference is doi: 10.1098/rstb.2014.0321. The one you gave leads to the article by Williams and Embley from the same issue ("Changing ideas about eukaryotic origins").
Thanks a bunch. I now have an earworm:
Symb eat oats, you carry oats, and eocyte eat ivy.
Thanks. Fixed.
Does anyone have a pre eukaryotic evolutionary identification of genes that could be a pre curser to the spliceosome or any of its parts?
It's good to know that the Archaean small subunit looks like a duck. If it can be determined that it also walks like a duck and quacks like a duck, we'll really get somewhere.
So why is the green segment of the ring joining up with eukaryotes only once, and why as sister group to Cyanobacteria? Shouldn't there be two arrows, one from Proteobacteria to the eukaryote stem and one from Cyanobacteria to the plant stem (as it were)?
Perhaps this could contain what you are looking for? Origin and evolution of spliceosomal introns.
The title of his paper is simply, "Eukaryotic origins" (Lake, 2015) and it's very fitting that it's the first paper since the current consensus is that he was right all along and the Three Domain Hypothesis is dead. Vindication.
The problem is that despite being called "the eocyte hypothesis" it isn't very much like what Lake proposed in the 1980s. The TACK clade clearly is still archeal, whereas the original eocytes were proposed as being something else entirely.
The advantage of a tree like this is that it doesn't rely on sequence data and that's a huge advantage because it avoids the main artifact of deep-rooted trees; namely, the long-branch attraction artifact
That was traditionally an argument of those favoring morphological trees, but it ignores that morphology is very subjective. When I was in grad school in the 1990s, people were still making phylogenic trees of birds based on the feather shape, but even such "naturalists" use molecular methods now.
Harumpf! I still like the domains as classifications (not phylogenetic units.) However, I have dutifully printed the nicely colored diagram, looked up articles in the Transactions and definitions in Wikipedia, and set out to learn more about prokaryotes than I every wanted to know. (It didn't take long to achieve that level of knowledge!)
You trying to say Jim Lake is a quack?
I'll get my coat...
Yes, I don't like how the photosynthetic lineage meets the eukaryotes either, though this is more symmetrical and thus prettier.
Shouldn't there be two arrows...
I wanted to ask the same question. Where are my mitichondria? And why am I getting plastids instead?
this is more symmetrical and thus prettier
If it's drawn this way, you can call it the Ring of Life rather than the Tangled Knot of Life.
Good question, the way this "tree" is drawn one could get the impression animal eukaryotes are derived eukaryotes that lost their photosynthetic organelles when they split from the common ancestor they share with plants.
The spaghetti of life. Praise unto his noodly appendages!
RAmen!
I expected you to post a comment within one hour.What took you so long?
If the TACK clade is still Archeal, does that mean the eukaryotes are Archael as well? Or is the TACK clade + Eukaryotes something different?
Thanks Mikkel
I have seen this paper but will re read.
Yes, TACK suggests that eukaryotes are archaeal. While you can argue that this is technically different from the traditional three domains, it isn't that much of difference from the rooted three domain tree. It's a lot closer to that than to what Lake proposed in 1984. Lake has the advantage of simply outliving Woese, which is one way of getting the last word in.
I'm somewhat confused. The text in the box says Eukaryota and Eocyta are sister taxa within Karyota. But if TACK is just a synonym of Eocyta, then Eukaryota (or at any rate the primaeval "host cell") is nested inside it, as the sister taxon of the Lokis (or so it seems at present -- things are developing really fast). That would mean that Karyota = Eocyta = TACK, or am I missing something?
Let's see how this figure is going to evolve by subtle LGT (Lateral knowledGe Transfer) of other people's ideas.
Traditionally Lake reserved "karyotes" for his hypothesized ancient proto-eukaryotes and "eocytes" for their closest living relatives. It isn't clear what he means these days, though. I agree that it looks like Karyota = Eocyta = TACK in his scheme.
Given what I've read(including that paper), what seems most plausible to me is that introns emerged as another type of selfish genetic elements(ala transposons), greatly enabled by the larger energy budget pr. gene of eukaryotes compared to prokaryotes.
But since coding region insertions are much more likely to be detrimental than between-gene insertions by things like transposons, the spliceosome, in this view, would have emerged and gradually coevolved with the proliferation of intron insertions largely driven by natural selection to compensate for insertions in coding regions.
This would seem to entail that only relatively few spliceosomal RNAs and proteins are derived from prokaryote ancestors to eukaryotes, if any. I think the vast majority of the spliceosome is effectively a giant adaptation of (and almost entirely unique to) eukaryotes to intron invasion.
The current prevalent view is that the splicing machinery, which is one of the most complex eukaryal macromolecular machineries, evolved as a defense mechanism against insertional mutagenesis ( http://biorxiv.org/content/biorxiv/early/2013/11/18/000588.full.pdf)
I can only reiterate my comment on the last thread on the ring of life. To me lateral gene transfer is not a reason to stop classifying into lineages, just like somebody who gets a liver transplant doesn't generally list the donor as their ancestor.
People have debated a lot whether the ribosome should be given a privileged place or not. I am firmly of the opinion that it should -- what makes a cell a cell is the autonomous capacity to synthesize proteins. So eukaryotes can be a chimera, and one in which the bacterial genes have come to dominate in numbers over the contribution of the original host, but the information-processing machinery can still define a lineage of ancestry.
Claudiu,
Thanks for the link. It is a molecular machine that appears to have changed several times over evolutionary history. I am interested in its role in enabling multi cellular evolution through alternative splicing.
... but the information-processing machinery can still define a lineage of ancestry.
Why?
Do you know how many of those genes actually show eukaryotes more closely related to Archaea than to Eubacteria? Which of the DNA polymerase genes define a lineage? Which of the genes for subunits of RNA polymerase define a lineage?
Hardly any of the genes for ribosomal subunits work at defining a lineage. How many of the chaperone genes support Three Domains?
Why wouldn't the genes for the various subunits of pyruvate dehydrogenase or the genes for the subunits of Complexes I, III, and IV work for defining lineages? Or the genes for the subunits of ATP synthase?
When the Three Domain Hypothesis started to collapse, its supporters looked around for something to salvage their hypothesis and they decided that they would award special privileges to those genes that give the "correct" tree. Some of them were "information-type" genes (especially one of the ribosomal RNA genes) so they decided that those genes were the ones that really told you the truth about the origin of eukaryotes.
I am familiar with the complications. I am talking about the whole system.
Also, I don't see why we have to argue over this when I don't think we disagree.
Anybody who knows about endosymbionts understands why information genes are central. An organism can lose almost all of its metabolic genes and do just fine (take a look at Mycoplasma for instance). But it can't lose its information processing genes and be a living organism.
The only point a creationist can make here is on the anatomy of the contention.
There was a original opinion and then a critic and then a response that seemed to go beyond academic disagreement. in short got personel. Then a victory over the former dominate opinion.
O see this all the time and am sure its the norm.
THe ID/YEC revolution is the critic, gets messed with, but will prevail in our times.
Opinions of people, tailless primates for some, are wrong in the beginning more then not. Unless there is revealed truth like from the bible.
Are you saying that an organism can lose the genes involed in making proton pumps, lipids, carbohydrates, amino acids, and nucleotides and still be a living organism?
Note that I don't care about the three domain hypothesis. My point is simply that I don't see why, for example, the lineage from eukaryotic cells that didn't have a bacterial endosymbiont to eukaryotic cells that had acquired a bacterial endosymbiont a few million years later should be considered a part of a network with the bacteria as opposed to simply a tree branch going from eukaryotic cells that didn't have a bacterial endosymbiont to eukaryotic cells that had acquired a bacterial endosymbiont.
Good points, Robert. But I think you have a typo in the last sentence. A creationist mentioned to me the other day that the bible is quite flawed in fact, and it is the Quran that is the only source of inerrant truth.
To me lateral gene transfer is not a reason to stop classifying into lineages, just like somebody who gets a liver transplant doesn't generally list the donor as their ancestor.
If the genetic basis of that transplanted liver persisted in the lineage of the recipient, then the offspring would be quite justified in including the original donor as an ancestor, no? We are not talking about one-off endosymbiotic events here (as you know), but fixed (more or less) attributes.
Mycoplasma genitalium can make *no* amino acids -- it gets them as well as most of its lipids from the environment (being a pathogen its environment is quite rich). And the "synthetic organisms" (generally modified Mycoplasmas) being created at JCVI and other institutions have even fewer metabolic genes
Likewise in the case of the only known parasitic archeon, Nanoarchaeon equitans:
The N. equitans genome (490,885 base pairs) encodes the machinery for information processing and repair, but lacks genes for lipid, cofactor, amino acid, or nucleotide biosyntheses. [Waters et al. 2003]
The genes for several vital metabolic pathways appear to be missing in Nanoarchaeum [1]. This could be due to two plausible reasons. N. equitans might represent an ancient species, and hence possesses a small genome. Alternatively, it might have gone through a process of genome reduction as a strategy of adaptation to the obligatory parasitic lifestyle, as observed in cases of many other parasitic/symbiotic organisms [1]. However, in obligatory intracellular bacteria, many genes involved in DNA recombination and repair along with the biosynthetic and metabolic genes are usually lost [3,4]. But N. equitans possesses most of the DNA repair enzymes and the complete genetic machinery necessary for transcription, translation and DNA replication. The complexity of its information processing systems and the simplicity of its metabolic apparatus, therefore, suggest the presence of an unanticipated world of organisms yet to be characterized. [Das et al. 2006]
Sorry, -aeum, not -aeon..
@Piotr
I understand your point when you're talking about non-free-living organsims that survive as parasites.
N. equitans might represent an ancient species, and hence possesses a small genome.
Are they suggesting that ancient species could make DNA, RNA, and protein but not lipids, cofactors, amino acids, and nucleotides?
What about viruses, some of which have more genes then many prokaryotic or eukaryotic cellular species? Aren't they living organisms?
SRM,
No, this is precisely where I disagree. The ancestors would still be the line of mothers and fathers from generation to generation, even if lateral gene transfer happened. I have a hard time seeing some retrovirus that inserted DNA into my ancestor a few million years ago as another one of my ancestors, for example.
Viruses aren't living organisms because they can't replicate themselves without a cell to use. While microbes with highly reduced genomes generally live parasitically as well in nature, they can live independently in sufficiently rich media.
I am fascinated by large viruses like Pandora and Mimi myself, but they aren't living organisms any more than any other virus are. The question obviously at this point is whether they evolved from small viruses picking up genes or if they evolved from independent organisms that lost even more of their genomes than did endosymbionts.
Are they suggesting that ancient species could make DNA, RNA, and protein but not lipids, cofactors, amino acids, and nucleotides?
The authors seem to be prepared to consider this. It sounds absurd to me (as opposed to the other possibility).
By the way, I have recently read that Pelagibacter, arguably the most abundant organism on this planet (or at least a strong contender for the title) is a close cousin of the mitochondrion ancestor -- they could even be treated as sister taxa, according to some analyses. Pelagibacter has the smallest genome of all free-living life forms, but it can make twenty amino acids and most of the common cofactors. One hypothesis about the evolution of alphaproteobacteria is that the common ancestor of Rickettsiales (including the proto-mitochondrion) was an endosymbiont (of the eocyte ancestor of Eukaryota?), and that Pelagibacter reverted to a free-swimming lifestyle after its genome had undergone slimming down in the intracellular environment, but before it lost any of its essential metabolic genes to the host's nuclear genome. I suspect, however, that its incredibly vast population (measured in octillions, no less) may be a sufficient explanation of the extremely streamlined genome.
That sounds extremely far fetched to me, and also unnecessary as a hypothesis - Pelagibacter is by no means so reduced that such explanation should be needed to understand its genome. The mitochondria originated 1.5-2 billion years ago, which is vastly more time than what is needed to streamline a free-living organism's genome
The genome of Pandoravirus salinus is 2.5 megabases and encodes approximately 2500 proteins, including some that are involved in translation (e.g. amino acid-tRNA ligases, eIF4E translation initiation) and several tRNAs.
Bacterium Carsonella ruddii has a genome 160 kilobases, which encodes approximately 180 proteins. Nasuia deltocephalinicola, which was recently discovered, has an even smaller genome at 112,091 nucleotides.
Are these bacteria living organisms?
I've found that article.
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3177885/
It looks like it would do some people a lot of good if they spent a little time hanging out in the blogosphere before they publish their ideas.
Note who the senior author of the paper is
Are these bacteria living organisms?
There's no sharp demarcation line between an obligate endosymbiont and an organelle of endosymbiotic origin.
Note who the senior author of the paper is
That's why I assumed their findings and analysis could be trusted. But of course dicussing one's ideas with other people (including less famous but knowledgeable colleagues) doesn't hurt and nobody should be above it.
Jonathan Badger, Saturday, September 05, 2015 10:10:00 AM:
I am fascinated by large viruses like Pandora and Mimi myself, but they aren't living organisms any more than any other virus are. The question obviously at this point is whether they evolved from small viruses picking up genes or if they evolved from independent organisms that lost even more of their genomes than did endosymbionts.
As I mentioned above, there are dozens of prokaryotic and eukaryotic species with genomes smaller than the genome of Pandoravirus salinus. And, as you wrote, it is likely that they evolved form free living ancestors that lost some of their genes. Let's hypothesize that Pandoravirus salinus evolved from a free-living ancestor; does it make sense in that case to consider it a living organism?
That's why I assumed their findings and analysis could be trusted
Are you sure you did not mean "couldn't"? There is a long history of wacky papers coming from that group. It has also produced a lot of important papers, but when you publish >2000 of them, even if the percentage of crap is in the single digits, it's still quite a few papers...
I am fascinated by large viruses like Pandora and Mimi myself, but they aren't living organisms any more than any other virus are. The question obviously at this point is whether they evolved from small viruses picking up genes or if they evolved from independent organisms that lost even more of their genomes than did endosymbionts.
Looks like they are just bloated NCLDVs
http://www.ncbi.nlm.nih.gov/pubmed/25042053
Are you sure you did not mean "couldn't"?
Well, I'm only a dilettante with a strong interest in the field but no insider's knowledge. I associate Raoult and his group with spectacular things like Mimi and virophages. Any details of their wacky side?
You posted one of them
I remember this one too:
http://www.biologydirect.com/content/pdf/1745-6150-6-55.pdf
Also, the Koonin paper about the NCLDVs is a response to Raoult papers proposing that giant viruses constitute a fourth domain.
Then you may want to read this:
http://www.sciencemag.org/content/335/6072/1033.long
Oh, I see what you mean. Thanks!
Although, similar to their free-living relatives, the intracellular parasitic or endosymbiotic cellular species do occasionally acquire new genetic material, there is overwhelming evidence that, overall, all these thousands of species have evolved by reductive evolution towards smaller genome and complexity. This is a fully accept fact by the all researchers in the field.
So, if all the intracellular parasitic or symbiotic cellular lineages have evolved overall by reductive evolution, why would parasitic or symbiotic viral lineages evolve the opposite way towards larger genomes and higher complexity?
I have a hard time seeing some retrovirus that inserted DNA into my ancestor a few million years ago as another one of my ancestors, for example.
Well, but they are. As are the ancestal bacteria and archaea that contributed to the eukaryotic genome. As for later examples of LGT, these may well be minor contributors to your ancestry but they have all contributed to what we are - essentially composite organisms (even if a lot of the DNA is non-functional now). That's how I (a non-expert in genomic biology and evolution) think about it anyway. I could be off the mark.
As I mentioned above, there are dozens of prokaryotic and eukaryotic species with genomes smaller than the genome of Pandoravirus salinus. And, as you wrote, it is likely that they evolved form free living ancestors that lost some of their genes. Let's hypothesize that Pandoravirus salinus evolved from a free-living ancestor; does it make sense in that case to consider it a living organism?
Again, "being a living organism" implies being able to replicate without needing another cell to reprogram, and has nothing to do with genome size. Yes, many living organisms don't live on their own in nature, but they can replicate on their own given the right growth media. If it can be shown that Pandoravirus can do that as well, I'd gladly accept it as a living organism. But not without it this evidence,
@SRM
If I may add my humble opinion to your discussion.
I think the only thing you have shown is that the concept of ancestry is fuzzy - like the concept of species.
Everybody will agree, that my parent are my ancestors. They contribute roughly the same amount of DNA to me. But retrovirus contributes only very small amount of DNA. It's hardly an ancestry.
Unless you define it that way. But I don't think it's good idea.
Of course in the case of the symbiosis of archebacteria and eubacteria it's more complicated. But I don't know much enough to say anything about it - I only wanted to make a minor point about ancestry.
Let's put on the side the question whether viruses are living entities or not, as it has been addressed for more than a century without a resolution. The elephant in the room in the exciting field of viral origin and evolution is the issue outlined above:
If all intracellular parasitic or symbiotic cellular lineages have evolved overall by reductive evolution, why would parasitic or symbiotic viral lineages evolve the opposite way towards larger genomes and higher complexity?
Ancestry is a fuzzy word, in terms of its usage, but it shouldn't necessarily be so in terms of the origins of our genome. Recognizing the composite nature of the human genome need not dull conventional usages of the word ancestry. But I won't say any more on the matter because if I did, I would increasingly feel more silly in an area where so many people know so much more than me.
Jonathan Badger,
I don't think you are offering a useful definition of what a living organism is. Viruses can replicate in cell-free systems, for example. Are those viruses that do this classed as living entities, while those that can't as non-living?
The growth medium in such cases is admittedly more complex, but that's not really relevant to the point. If Wolbachia[ can be rescued from the charge of being non-living by artificial means then it's only fair that we allow the same standards for viruses.
'The current prevalent view' or 'my personal view'?
Claudiu,
"If all intracellular parasitic or symbiotic cellular lineages have evolved overall by reductive evolution, why would parasitic or symbiotic viral lineages evolve the opposite way towards larger genomes and higher complexity?"
A good question. Since it seems to have happened, why do you think it happened?
@DAK
Those "cell-free" viral replication systems work by providing most of the enzymatic machinery of a cell. That's not the same thing as just providing a rich media for auxotrophs. If you are allowed to introduce such machinery to allow replication, what *isn't* alive? You can replicate any DNA molecule in cell-free systems (that's how PCR works). So is all DNA alive?
Exactly. Under this scenario, the definition of living is dependent upon the complexity of the growth medium. Such an approach will run into all sorts of trouble with borderline cases - both real and speculative - as you have illustrated.
DAK - Jonathan is referring to something akin to an in vitro transcription-translation system which is very different from identifying a growth medium in which a virus can replicate.
Also, is there any evidence that Wobachia can replicate outside of host cell. I see a paper talking about maintaining viability outside of the cell for a time, but not replication. I found a thesis that claimed Wolbachia would also replicate in a growth medium, but I dont see where that was ever published in a journal - quick look on my part, I might have missed something in the literature.
I'm not sure if people have succeeded in replicating Wolbachia in media, but unlike with viruses there is no theoretical reason for this. Creating appropriate media is still more of an art than a science. Even most free-living bacteria haven't been successfully grown in culture.
Chris B Sunday, September 06, 2015 12:01:00 AM:
"If all intracellular parasitic or symbiotic cellular lineages have evolved overall by reductive evolution, why would parasitic or symbiotic viral lineages evolve the opposite way towards larger genomes and higher complexity?"
A good question. Since it seems to have happened, why do you think it happened?"
Well, I don't think it happened. It makes no biological sense to think that viruses evolved towards larger genomes and higher complexity within an intracellular environment. If there are laws in Biology, this is one of them: no parasitic species evolves towards complexity in an intracellular environment.
Claudiu.
"Well, I don't think it happened. "
What are your hypotheses then, for how large genome viruses evolved? They exist, so in fact they did happen. How did they get here?
"It makes no biological sense to think that viruses evolved towards larger genomes and higher complexity within an intracellular environment. If there are laws in Biology, this is one of them: no parasitic species evolves towards complexity in an intracellular environment."
'Biological sense' is often too inflicted with anthropomorphic thinking, and adopting it as a default hypothesis is very dangerous. The biological "law" you pronounce is by no means a law. Taking your parameters of "larger genomes" and "higher complexity", present some specific examples to discuss,
Chris B:
Good catch -- NCLDVs in fact repeatedly evolved into large-genome varieties. So it's not even just a single example...
Georgi,
Yes, there are several examples. Viruses are not bacteria, and as Jonathan Badger pointed out earlier in this thread, there is a difference between taking over metabolic machinery of a cell like viruses can do, and losing the ability to synthesize certain necessary metabolic components (like auxutrophic bacteria), and obligately intracellular parasites like Rickettsia.
Chris B, Monday, September 07, 2015 11:09:00 PM:
What are your hypotheses then, for how large genome viruses evolved? They exist, so in fact they did happen. How did they get here?
You can find recent presentation of my hypothesis here: http://precedings.nature.com/documents/3886/version/1/files/npre20093886-1.pdf
'Biological sense' is often too inflicted with anthropomorphic thinking, and adopting it as a default hypothesis is very dangerous
I meant ‘biological sense’ in the sense of ‘common sense’, just as articulated by Peter Medawar many years ago: “The scientific method is a potentiation of common sense, exercised with a specially firm determination not to persist in error”
Georgi Marinov, Monday, September 07, 2015 11:11:00 PM:
"Good catch -- NCLDVs in fact repeatedly evolved into large-genome varieties. So it's not even just a single example..."
Exactly, that's the 'Elephant in the Room' of the exciting field of viral origin and evolution:
According to the prevalent view on the origin and evolution of viruses, numerous viral lineages evolved towards larger genomes and higher complexity, although there is no solid data supporting this view. On the contrary the current data clearly indicates that, without exception, the tens of thousands of intracellular parasitic cellular species have evolved by reductive evolution from more complex free living species.
Without addressing this obvious dilemma, the current prevalent view about the origin and evolution of viruses is questionable.
How exactly does the evidence point to that?
Point to what?
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