Eukaryotes' Closest Relatives?

[lpetrich]

Among cellular organisms, the most obvious difference in cell structure is between prokaryotes (before nuclei) and eukaryotes (true nuclei), between cells without nuclei and cells with nuclei. Eukaryotic cells have a lot of structure that prokaryotic ones lack, like cell nuclei and various organelles.

Since the late 19th cy., various people have speculated that some eukaryote organelles are descendants of outside organisms that took up residence in their host cells ( Symbiogenesis), and this notion was revived in the mid-1960's by Lynn Petra Alexander Sagan Margulis (yes, she was Carl Sagan's first wife). Over the 1970's, it became well-established for two kinds of organelles, mitochondria and chloroplasts. Mitochondria turned out to be closest to alpha-proteobacteria, like root-nodule bacteria and rickettsia bacteria, and chloroplasts to cyanobacteria, formerly called blue-green algae.

The rest of the cell's origin has been a much more difficult problem.

First some background. In the 1970's, a deep split in prokaryotes was discovered, between Bacteria or Eubacteria, and Archaea or Archaebacteria. Bacteria contains most of the better-known prokaryotes, including all pathogenic ones and the ancestors of mitochondria and chloroplasts, and Archaea contains a lot of oddballs, like methanogens (they do CO2 + 4H2 -> CH4 + 2H2O), and many hydrothermal-vent organisms. Some of them are hyperthermophiles, living in very high temperatures like above the boiling point of water at sea level.

Eukaryote informational systems turned out to resemble those in Archaea and their metabolic genes those in Bacteria. Their membrane lipids contain fatty acids, like in Bacteria, instead of terpenes, like in Archaea.

But for a long time, no archaea seemed especially close to Eukarya. Did the ancestors of present-day Archaea diverge from the ancestor of the eukaryote informational system early in the history of our planet's biota?

 

[lpetrich]

The Bacteria-Archaea split was proposed in 1977 by Carl Woese and George E. Fox, and to this day, it remains the earliest known split in the family tree of our planet's biota.

Of its subtaxa, Euryarchaeota and Crenarchaeota were proposed in 1990, making Archaea split into Eury and Cren. Then Korarchaeota was proposed in 1996, Thaumarchaeota in 2008, and Aigarchaeota in 2011, and all but Eury united as TACK in 2011, making Archaea split into Eury and TACK as its main subgroups.

In 2013, a taxon named DPANN was proposed as a supergroup of 5 taxa. Its relation with Eury and TACK is not very clear. I've seen (DPANN, (Eury, TACK)) and DPANN as a subtaxon of Eury.

During this time, eukaryotes' informational systems were typically found to be most closely related to Archaea as a whole or else to TACK.

Then in 2015, a remarkable discovery was made near a hydrothermal vent that someone named Loki's Castle, a hydrothermal vent on the Mid-Atlantic Ridge near Norway, Svalbard, and Greenland. It was made by sequencing DNA from nearby ocean-floor mud. Such environmental-DNA sequencing had already been done for several years, something made possible by high-throughput gene sequencing: Metagenomics: DNA sequencing of environmental samples | Nature Reviews Genetics (2005).

The discoverers found genetic material that they could recognize as coming from some archaeon, some member of Archaea, and they named this putative organism Lokiarchaeum, in honor of where it was found. But it was an odd one, not closely related to any of the others, and one with some distinctively eukaryotic genes in it. These genes did not seem to be from contamination, since they were flanked by prokaryotic genes.

Lokiarchaeum gave its name to the taxon Lokiarchaota, and similar organisms were soon discovered. Thorarchaeota in 2016 and Odinarchaeota and Heimdallarchaeota in 2017. Their supertaxon was then named Asgard or Asgardarcheota, continuing the Norse-mythology naming theme.

Their closest relatives are the TACK organisms, making a supertaxon, Proteoarchaeota.

The relationships of Eury, DPANN, and Proteo are not very clear.

Also not very clear is the Asgard - Eukarya relationship. Are the eukaryotes closest to Asgard as a whole? Or some members of Asgard? Or more properly, eukaryote informational systems.

 

[lpetrich]

Then a year ago, some researchers succeeded in growing an Asgard microbe in their lab. Isolation of an archaeon at the prokaryote–eukaryote interface | Nature

It took the researchers several years to grow usable quantities of Asgard microbe, a strain that they named MK-D1. Compared to other one-celled organisms, this organism is very slow-growing, with a doubling time of some 14 to 25 days.

"After six transfers, MK-D1 reached 13% abundance in a tri-culture containing a Halodesulfovibrio bacterium (85%) and a Methanogenium archaeon (2%)".

Organisms that MK-D1 lives in close association with.

"Through metagenome-based exploration of the metabolic potential of this archaeon and a stable-isotope probing experiment, we discovered that MK-D1 can catabolize ten amino acids and peptides through syntrophic growth with Halodesulfovibrio and Methanogenium through interspecies hydrogen (and/or formate) transfer".

That is, by exchanging nutrients. MK-D1 makes hydrogen that the others use.

"Through subsequent transfers, we were able to eliminate the Halodesulfovibrio population, enabling us to obtain a pure co-culture of the target archaeon MK-D1 and Methanogenium after a 12-year study—from bioreactor-based pre-enrichment of deep-sea sediments to a final 7 years of in vitro enrichment"

They have named MK-D1 Candidatus Prometheoarchaeum syntrophicum - the "candidatus" referring to the name's provisional status.

 

[lpetrich]

All that effort yielded amounts of MK-D1 microbes large enough to easily study.

The organisms are spherical (cocci) and very small, 300 - 750 nm in diameter, averaging 550 nm. They generally formed clumps. They had no organelle-like structures in them. They make strands about 100 nm in diameter, though they do not form elaborate networks or intercellular connections.

They have typical Archaea membrane lipids - terpenes - but not fatty acids.

The microbes can degrade amino acids anaerobically, and they release hydrogen as they do so.

"Locality. Isolated from deep-sea methane-seep sediment of the Nankai Trough at 2,533 m water depth, off the Kumano area, Japan." -- a long way from the North Atlantic.

The paper gives a phylogeny that was constructed with 31 ubiquitous ribosomal proteins. It goes

(Bacteria, Archaea: (Eury, (TACK, (MK-D1, Eukarya))))

with MK-D1 in Lokiarchaeota. Comparison to other Asgard organisms reveals that they also can live off of degrading amino acids, and that they also release hydrogen as they do so.

 

[lpetrich]

The researchers then describe how an organism much like MK-D1 could have become the ancestor of the eukaryotes.

This work is a little after this special issue: Journal of Theoretical Biology | The origin of mitosing cells: 50th anniversary of a classic paper by Lynn Sagan (Margulis) | ScienceDirect.com by Elsevier -- she published it in 1967

On the origin of mitosing cells: A historical appraisal of Lynn Margulis endosymbiotic theory - ScienceDirect

• Margulis’ scheme on eukaryogenesis by endosymbiosis was not a mere revival of old ideas.
• Her coherent evolutionary narrative provided testable hypotheses and specific predictions.
• Genome analyses strengthen the role of endosymbiosis in eukaryogenesis.
• The role of symbiosis in evolutionary innovation expands the Darwinian foundations.
• Margulis endosymbiotic scenario stands as a lasting scientific contribution.

So LM's work was a worthy start of research into this subject. She proposed three endosymbioses: of the mitochondrion, the chloroplast, and the flagellum. She proposed that eukaryote flagella are descended from spirochetes or some similar bacteria. Of these proposals, mitochondria and chloroplasts became accepted, in good part because of genomic evidence, but the eukaryote flagellum shows none of the sort of evidence that mitochondria and chloroplasts have of their outside origins.

Revisiting the theoretical basis of the endosymbiotic origin of plastids in the original context of Lynn Margulis on the origin of mitosing, eukaryotic cells - ScienceDirect

... However, the major part of her hypothesis, which she believed to be original, was the origin of mitosis.

... Whether the centriole-DNA complex originated from a spirochete or not was a minor anecdote in this initial postulate. Unfortunately, this hypothesis on the origin of mitosis, which she believed to be a holistic unity, testable by experiments, was entirely refuted.

But she deserves credit with coming up with an ingenious hypothesis.

 

[lpetrich]

Serial endosymbiosis or singular event at the origin of eukaryotes? - ScienceDirect

The last eukaryotic common ancestor now seems to have been essentially a modern eukaryotic cell that had already evolved mitosis, meiotic sex, organelles and endomembrane systems. The long search for missing evolutionary intermediates has failed to turn up a single example, and those discussed by Margulis turn out to have evolved reductively from more complex ancestors.

Some eukaryotes don't have mitochondria, but such "amitochondriate" organisms have genomic evidence of the former presence of these organelles.

"Instead, a modern synthesis of genomics and bioenergetics points to the endosymbiotic restructuring of eukaryotic genomes in relation to bioenergetic membranes as the singular event that permitted the evolution of morphological complexity."

That is, some singular event.

The CoRR hypothesis for genes in organelles - ScienceDirect - "Co-location for Redox Regulation" - that mitochondria and chloroplasts keep their genomes because that's the most convenient location for regulating the transcription of their genes.


Physiology, anaerobes, and the origin of mitosing cells 50 years on - ScienceDirect

• Margulis proposed that plastids and mitochondria arose in separate endosymbioses.
• She linked biological and geological history through a simple narrative about oxygen.
• Margulis's versions of endosymbiotic theory did not account for eukaryotic anaerobes.
• It has gone largely unnoticed that she proposed 20 independent origins of plastids.
• The spirochaete part of her theory was never supported by data.

...
The paper presented an appealing narrative that linked the origin of mitochondria with oxygen in Earth history: cyanobacteria make oxygen, oxygen starts accumulating in the atmosphere about 2.4 billion years ago, oxygen begets oxygen-respiring bacteria that become mitochondria via symbiosis, followed by later (numerous) multiple, independent symbioses involving cyanobacteria that brought photosynthesis to eukaryotes. With the focus on oxygen, Margulis's account of eukaryote origin was however unprepared to accommodate the discovery of mitochondria in eukaryotic anaerobes. Today's oxygen narrative has it that the oceans were anoxic up until about 580 million years ago, while the atmosphere attained modern oxygen levels only about 400 million years ago. Since eukaryotes are roughly 1.6 billion years old, much of eukaryotic evolution took place in low oxygen environments, readily explaining the persistence across eukaryotic supergroups of eukaryotic anaerobes and anaerobic mitochondria at the focus of endosymbiotic theories that came after the 1967 paper.

So LM proposed some 20 independent origins of chloroplasts from cyanobacteria. "Plastid" is a general term that covers the variety of colors that these organelles can have. But while she was correct about the ancestral kind of organism for chloroplasts, she was incorrect about how many times it happened. As far as we can tell, only once.

But eukaryotic algae have become "chloroplasts" for other eukaryotes, as "secondary" and "tertiary" endosymbiosis, as opposed to the single "primary" one of a cyanobacterium.

 

[Swammerdami]

Thanks Ipetrich! This is a topic I find very interesting. Lynn (Sagan) Margulis, BTW, was an avid fan of Lovelock's Gaia Hypothesis.

Clicking the links to read papers I hit pay-walls. This is OK; I find Nick Lane's books mostly good enough for my layman's use. And some papers were free to view:

Symbiogenesis: Beyond the endosymbiosis theory? — termites apparently evolved from cockroaches because of symbiosis with gut prokaryotes. The authors treat this as evidence supporting Margulis' hypothesis.

The CoRR hypothesis for genes in organelles — detailed look at mitochondria and chloroplasts, again supporting the work of Lynn Margulis

Life before LUCA — this useful paper is paywalled at ScienceDirect but available at http://bip.cnrs-mrs.fr/bip10/LUCA.pdf .


As Ipetrich mentions, it's good to remember that the amitochondrial eukaryotes are NOT a "missing link" in the early evolution of eukaryotes, but have evolved from eukaryotes WITH mitochondria. The gulf between the most complex prokaryote and the simplest eukaryote is HUGE.

 

[lpetrich]

In that special issue:
Symbiosis in eukaryotic evolution - ScienceDirect
by Purificación López-García, Laura Eme, David Moreira

About MK-D1:
Cultured Asgard Archaea Shed Light on Eukaryogenesis - ScienceDirect -- open access; not paywalled
by Purificación López-García, David Moreira

The first cultured Asgard archaeon lives in metabolic symbiosis with hydrogen-scavenging microbes. Its full-genome analysis authenticates the existence of Asgard archaea, previously only known from metagenome-assembled genomes, confirms their closer phylogenetic relatedness to eukaryotes and reinforces the idea that the eukaryotic cell evolved from an integrated archaeal-bacterial syntrophic consortium.

...
Rather, the prevalent scenario, inspired by Carl R. Woese’s proposal of three primary domains of life, invoked an independent proto-eukaryotic lineage sister to archaea that developed most typical eukaryotic traits (complex cytoskeleton, endomembranes, phagocytosis, nucleus, etc.) before it acquired the alphaproteobacterial ancestor of mitochondria.

But though some eukaryotes don't have mitochondria, it turned out that they lost those organelles rather than having never had them.

"Many Asgard eukaryotic-like genes encoded membrane-remodeling proteins, which promoted the hypothesis that eukaryotes evolved from a complex archaeon that developed endomembranes and phagocytosis." - the way that many protists eat, and a path for the proto-mitochondrion to get inside the cell.

But MK-D1 is not capable of phagocytosis, but instead eats in the usual prokaryote fashion, by absorption. It produces H2 rather than consuming it, contrary to what the archaeon does in the usual form of the "hydrogen hypothesis" of eukaryote origins.

Imachi et al., the discoverers of this strain, propose that some alpha-proteobacterium entered into a symbiosis with a MK-D1-like organism, consuming that organism's hydrogen output, and ending up being entangled and then pulled inside -- their Entangle-Engulf-Endogenize or E3 model.

 

[lpetrich]

But PLG and DM have a hypothesis of their own, their "revised syntrophy hypothesis", which they stated in The Syntrophy hypothesis for the origin of eukaryotes revisited | Nature Microbiology

It involved not two but three organisms, a MK-D1-like Asgard organism, an alpha-proteobacterium, and a delta-proteobacterium.

In it, both the archaeon and the alpha-proteo come to live inside the delta-proteo. The archaeon produces hydrogen, and the delta-proteo reduces sulfate to sulfide with it. The alpha-proteo then oxidizes the sulfide to sulfate with oxygen, thus completing this sulfur cycle.

This model explains why eukaryotes have eubacterial membrane lipids, with fatty acids, instead of archaeal ones, with terpenes. It also explains why the cell nucleus is surrounded by a membrane.

Making such big changes to membrane lipids seems difficult to do. "Indeed, no such transition has ever been observed and, although an engineered Escherichia coli strain can incorporate up to 30% archaeal phospholipids in its membrane, higher percentages of phospholipids impair growth and result in aberrant morphologies and asymmetric division (Caforio et al., 2018)."

Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane | PNAS

 

[lpetrich]

If terpenes make you think "turpentine", don't be surprised. Terpenes are named after turpentine, where they were first found.

Terpenes are found across both major branches of prokaryotes, and they are also well-represented in eukaryotes, like pine trees.  Terpene

But of prokaryotes, only eubacteria make fatty acids.

-

Life before LUCA - LUCA, however, is much older than the first eukaryote.

I found that paper to be very hand-wavy and not much of a contribution.

 

[lpetrich]

I'd posted back in 2016 on these close relatives of eukaryotes: Eukaryote Missing Link?

The overall phylogeny of eukaryotes has long been a difficult subject, complete with false starts along the way. The New Tree of Eukaryotes - ScienceDirect - January 2020 - describes some recent work on that subject.

The first molecular-phylogeny efforts, in the 1980's, with small-subunit ribsomal RNA (SSU rRNA), found that animals, plants, and fungi were well-defined groups that formed a "crown group". Outside that group were some protists that lacked mitochondria, like Giardia lamblia and Vairimorpha, a microsporidian. This had a clear implication for the evolution of mitochondria, that the ancestral mitochondrion was acquired by the ancestor of the crown group.

But when biologists sequenced some proteins for some of these organisms, they found different family trees, and they concluded that there is something called "long-branch attraction" that produces mistakes in family trees. Microsporidians turned out to be closely related to fungi, for instance.

Also, many mitochondrion-less protists turned out to have vestigial mitochondria like hydrogenosomes and mitosomes, and it's nowadays thought that mitochondria are ancestral to eukaryotes, with mitochondrion-ones having reduced or lost them.


By 2000, a system of five or six supergroups had emerged, though some of them did not survive very well in later work. Here is where we are at now. All these groups are strongly supported unless indicated otherwise.

Amorphea: (Opisthokonta, Amoebozoa)
Opisthokonta: ((animals, choanoflagellates), fungi)
Amoebozoa: lots of amoebas and slime molds
2000: Opi, Amo well-supported, Amo weakly supported back then

Its closest relative is likely CRuMs - a motley collection of protists united by molecular phylogeny

Discoba: (Euglenozoa, Heterolobosea, jakobids, Tsukubamonas) -- Euglenozoa contains Euglena
Metamonada: (Diplomonadida, Parabasalia, ...) -- Diplomonadida contains Giardia
2000: united as Excavata because of having a feeding groove. Excavata is poorly supported.

Haptista (haptophytes, centrohelids)

Cryptista (cryptomonads)

TSAR: (Telonemia, SAR)
SAR: ((Stramenopiles, Alveolata), Rhizaria)
Stramenopiles: (oomycetes, diatoms, golden algae, brown algae, ...) -- brown algae include kelp
Alveolata: (ciliates, apicomplexans, dinoflagellates, ...)
Rhizaria: (cercozoans, foraminiferans, radiolarians) -- mostly amoeboid, often with shells

The 2000 supergroup Chromalveolata included Stramenopiles, Alveolata, Haptista, and Cryptista. They were united by having plastids derived from red algae, but their nuclear genomes are too different, and that means separate acquisition of red algae or else protests with red algae as plastids -- Russian-doll endosymbiosis.

Rhizaria is also a 2000 supergroup, but unlike Chromalveolata it is enduring.

Archaeplastida (Chloroplastida, Rhodophyta, Glaucophyta) -- united by having a primary plastid, otherwise weak
Chloroplastida or Viridiplantae: (green algae, land plants)
Rhodophyta: red algae

Archaeplastida is a 2000 supergroup, but in some analyses, Cryptista is mixed in with the subgroups of Archaeplastida

 

[lpetrich]

There are plenty of protists that are not very close to any of the larger supergroups, like malawimonads, ancyromonads, hemimastigotes, ...

Not only red algae, but also green algae have become secondary plastids -- in Euglena and in chlorarachniophytes (host is in Cercozoa, Rhizaria, TSAR)


This rapid multiple divergence means that the root of the eukaryote family tree has been hard to discover. Even so, one can get a fairly good idea of what it was like. It was one-celled, it had mitochondria, chromosomes, mitosis, a meiosis-cell-fusion sexual cycle, and a flagellum, and it ate smaller organisms with phagocytosis, pulling in the cell membrane near its meal to make a bubble around it. It did not have photosynthesis.


A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids | Nature Communications

Those plastids are in Cryptophyta (Cryptista), Haptophyta (Haptista), Myzozoa (Alveolata), and Ochrophyta (Stramenopiles), where I list a containing taxon for each taxon of photosynthesizers.

The article mentioned hypotheses of endosymbiosis sequences, versions of a "rhodoplex" hypothesis:
Rhodophytina -> Cryptophyta -> Ochrophyta -> (Haptophyta, Myzozoa)
Rhodophytina -> Cryptophyta -> (Haptophyta -> Myzozoa), Ochrophyta

Rhodophytina = a subgroup of Rhodophyta, the red algae, along with Cyanidiophyceae

After noting fossil evidence of red algae in the Proterozoic from 1.2 billion years ago and possibly 1.6 Gya,

Evidence for the diversification of red algal plastid-containing lineages comes much later in the fossil record, which is apparent in the well-documented Phanerozoic continuous microfossil records starting from about 300 million years ago (mya). This period marks the diversification of some of the most ecologically important algae in modern oceans such as diatoms (ochrophytes), dinoflagellates (myzozoans) and coccolithophorids (haptophytes).

Dinoflagellates make deadly "red tides".

The red alga that became a plastid is inferred to be a "stem group" one and not a "crown group" one -- "crown group" is the minimum group that contains all present-day descendants and "stem group" is the maximum group that does not contain any other present-day descendants. One may add to "present day" with the fossil record if it is good enough.

Inferred ranges of dates for stem groups:

• Rhodophytina: 1675 - 1281 Mya
• Cryptophyta: 1658 - 440 Mya
• Ochrophyta: 1298 - 622 Mya
• Haptophyta: 1943 - 579 Mya
• Myzozoa: 1520 - 696 Mya

All these ranges of dates overlap, and they are consistent with versions of the rhodoplex hypothesis, including the two scenarios mentioned earlier.

The authors also found that Archaeplastida is a monophyletic group, with an ancestor and all its descendants, and also
((TSAR, Haptista), (Archaeplastida, Cryptista))

The Last Eukaryote Common Ancestor they found to have lived 2386 - 1958 Mya, near the beginning of the Proterozoic.

 

[lpetrich]

Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes | Paleobiology | Cambridge Core with a copy at pbio_26_303.386_404.tp - Butterfield2000PBiol-Bangiomorpha.pdf

A 1.2-billion-year-old fossil of a red alga:
Archaeplastida > Rhodophyta > Bangiophyceae > Bangiales > Bangiaceae > Bangiomorpha pubescens
closely resembling present-day Bangia

-

A one-billion-year-old multicellular chlorophyte | Nature Ecology & Evolution with a copy at Tang__2020__NEE__Green_algae_120200228-23174-1ykgjpj-with-cover-page-v2.pdf

A 1-billion-year-old fossil of a green alga:
Archaeplastida > Chloroplastida > Chlorophyta > Ulvophyceae > Siphonocladales > Proterocladus antiquus

-

Early fungi from the Proterozoic era in Arctic Canada - PubMed about 1.01 - 0.89 billion years ago

Glomalean fungi from the Ordovician - PubMed - the earlier champion, at around 460 million years ago

 

[DrZoidberg]

Among cellular organisms, the most obvious difference in cell structure is between prokaryotes (before nuclei) and eukaryotes (true nuclei), between cells without nuclei and cells with nuclei. Eukaryotic cells have a lot of structure that prokaryotic ones lack, like cell nuclei and various organelles.

Since the late 19th cy., various people have speculated that some eukaryote organelles are descendants of outside organisms that took up residence in their host cells ( Symbiogenesis), and this notion was revived in the mid-1960's by Lynn Petra Alexander Sagan Margulis (yes, she was Carl Sagan's first wife). Over the 1970's, it became well-established for two kinds of organelles, mitochondria and chloroplasts. Mitochondria turned out to be closest to alpha-proteobacteria, like root-nodule bacteria and rickettsia bacteria, and chloroplasts to cyanobacteria, formerly called blue-green algae.

The rest of the cell's origin has been a much more difficult problem.

First some background. In the 1970's, a deep split in prokaryotes was discovered, between Bacteria or Eubacteria, and Archaea or Archaebacteria. Bacteria contains most of the better-known prokaryotes, including all pathogenic ones and the ancestors of mitochondria and chloroplasts, and Archaea contains a lot of oddballs, like methanogens (they do CO2 + 4H2 -> CH4 + 2H2O), and many hydrothermal-vent organisms. Some of them are hyperthermophiles, living in very high temperatures like above the boiling point of water at sea level.

Eukaryote informational systems turned out to resemble those in Archaea and their metabolic genes those in Bacteria. Their membrane lipids contain fatty acids, like in Bacteria, instead of terpenes, like in Archaea.

But for a long time, no archaea seemed especially close to Eukarya. Did the ancestors of present-day Archaea diverge from the ancestor of the eukaryote informational system early in the history of our planet's biota?

They're more than relatives. We're an Eukaryotic species

 

[lpetrich]

Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae


Palaeos Proterozoic: The Proterozoic Era - has a section on "acritarchs", microfossils of organic material that are often interpreted as one-celled eukaryotes, usually as one-celled algae -  Acritarch

From Palaeos, "In general they verify the that, after an initial burst of diversification in the later Paleoproterozoic, development was gradual or even static until the Neoproterozoic."
"later Paleoproterozoic" ~ 1.7 billion years ago, "Neoproterozoic" began 1 billion years ago.


Timing the origin of eukaryotic cellular complexity with ancient duplications

Eukaryogenesis is one of the most enigmatic evolutionary transitions, during which simple prokaryotic cells gave rise to complex eukaryotic cells. While evolutionary intermediates are lacking, gene duplications provide information on the order of events by which eukaryotes originated. Here we use a phylogenomics approach to reconstruct successive steps during eukaryogenesis. We found that gene duplications roughly doubled the proto-eukaryotic gene repertoire, with families inherited from the Asgard archaea-related host being duplicated most. By relatively timing events using phylogenetic distances we inferred that duplications in cytoskeletal and membrane trafficking families were among the earliest events, whereas most other families expanded predominantly after mitochondrial endosymbiosis. Altogether, we infer that the host that engulfed the proto-mitochondrion had some eukaryote-like complexity, which drastically increased upon mitochondrial acquisition. This scenario bridges the signs of complexity observed in Asgard archaeal genomes to the proposed role of mitochondria in triggering eukaryogenesis.

It must be noted that there is a complicating factor. Evidence of gene duplication is best preserved if the duplicated genes then become specialized in different directions. Otherwise, one of the genes is likely to become disabled by a mutation that does not get selected against because another one is still functional.

 

[lpetrich]

Back to eukaryotic phylogeny.

There's a grouping called Obazoa: Opisthokonta with some additional protists, Breviatea and Apusomonadida.
"Obazoa" looks like an acronym of its members with -zoa, since most of the protists in it are animal-like: protozoa.

In turn, Obazoa is in Amorphea alongside Amoebozoa.
Amorphea is formerly the unikonts from how many flagella, but that turns out to be a misnomer.


Another grouping that has emerged over the last decade is Diaphoretickes: Archaeplastida, Cryptista, Haptista, TSAR, some extra protists

There are some further ones that have recently been proposed:

• Opimoda (formerly Unikonta): Amorphea, CRuMs
• Diphoda (formerly Bikonta): Diaphoretickes, Discoba

Metamonada is hard to place.


When searching for Opimoda and Diphoda, I found this: Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life | PNAS
Referring to the meiosis-fusion cycle -- it is scattered across eukaryotedom, meaning that it was inherited from the ancestral eukaryote.

 

[lpetrich]

Turning to prokaryote phylogeny, that was even more difficult than overall eukaryote phylogeny, where one could infer that multicellularity evolved several times. There also, it took gene sequencing to get a good idea of it. The first molecule sequenced to get a good idea of prokaryote phylogeny was the one for overall eukaryote phylogeny: small-subunit ribosomal RNA, selected because of its ubiquity in cellular organisms. But sequencing was not very well-developed in the early 1970's, so Carl Woese and his colleagues used the expedient of snipping up with enzymes this roughly 1500-nucleotide molecule. They would then sequence the pieces and compare the resulting sequence catalogs.

At first, they found the expected split between prokaryotes and eukaryotes. But then one day ... BANG! They sequenced a methanogen and it was about as far from the other prokaryotes as the eukaryote. As they continued their sequencing, they found three groups of sequences: most prokaryotes, prokaryotes like that methanogen, and eukaryotes. That's what led to the concept of three domains: Bacteria, Archaea, and Eukarya. But it's now evident that Eukarya originated from Bacteria and Archaea, and the Bacteria-Archaea split continues to be the earliest-known split in the phylogeny of our planet's biota.

But as more and more genes became sequenced, it became evident that prokaryotes have exchanged large numbers of genes among themselves, lateral gene transfer or horizontal gene transfer. There is so much of it that some biologists have doubted that a family tree of them is very meaningful -- only family trees of their component genes. But one can nevertheless construct average-over-genes phylogenies, or else use informational genes for a reference phylogeny.

Recent work has improved the bacterial-phylogeny resolution, with some recent work identifying two main clades that contain most of the ordinary bacteria:  Terrabacteria and  Gracilicutes ("slender skins", from having relatively thin cell walls). A rooted phylogeny resolves early bacterial evolution | bioRxiv

Terrabacteria contains bacteria with adaptations for living on dry land, like thick cell walls, walls that react with the Gram stain for identifying bacteria. This taxon contains Cyanobacteria ("blue-green algae") and two Gram-positive taxa: Firmicutes ("strong skins") and Actinobacteria, formerly known as actinomycetes. Firmicutes includes spore-forming bacteria, with the spores being for surviving dryness.

Gracilicutes contains Proteobacteria, a taxon with the likes of Escherichia coli, Salmonella, legume root-nodule bacteria, and rickettsias.

 

[lpetrich]

It looks like there was a lot of evolution between the First Eukaryotic Common Ancestor (FECA) and the Last Eukaryotic Common Ancestor (LECA).

The FECA was some Asgard archaeon, and there was a lot of evolution between it and the LECA, notably the acquisition of the mitochondrion, and the development of the endomembrane system, eukaryotic cell signaling, and the eukaryotic cell cycle, including meiosis and cell fusion.

The  Endomembrane system is a variety of structures of eukaryotic cells: the nuclear membrane, the endoplasmic reticulum, the Golgi apparatus, lysosomes, vesicles, endosomes, and the plasma (cell) membrane.

That means that there was some burst of evolution that has no known non-LECA descendants. But there might have been. Numerous protists have been discovered to be only distantly related to other eukaryotes, as far from them as they are from each other. Could some of them be non-LECA descendants?

One has to ask why the difficulty. Could these proto-eukaryotes have lived much like their Asgard ancestors before they acquired some ability that made them break out of their original niche? What breakout ability might that have been? I'm speculating phagocytosis, eating by engulfing one's food. That involves pulling it into the cell with a cell-membrane bubble surrounding it. Then the cell squirts digestive enzymes into the bubble and absorbs the digested food. Anything remaining is disposed of by moving the bubble back to the surface and opening it to the outside world.

The digestive enzymes were pre-existing, since they are used in proteasomes, protein recycling centers that are found in most cellular organisms. They work by taking in proteins then cutting them up with digestive enzymes. The resulting amino acids are then returned to the rest of the cell.

Phagocytosis is common among one-celled heterotrophic eukaryotes, though not a common form of digestion among multicellular ones. However, most animals have kinds of cells that dispose of unwanted organisms by doing phagocytosis on them.

Phagocytosis is IMO a good candidate for that breakout capability because it could have made possible much higher-quality nutrition, thus the ability to colonize many more environmental niches.

Timing the origin of eukaryotic cellular complexity with ancient duplications

Eukaryogenesis is one of the most enigmatic evolutionary transitions, during which simple prokaryotic cells gave rise to complex eukaryotic cells. While evolutionary intermediates are lacking, gene duplications provide information on the order of events by which eukaryotes originated. Here we use a phylogenomics approach to reconstruct successive steps during eukaryogenesis. We found that gene duplications roughly doubled the proto-eukaryotic gene repertoire, with families inherited from the Asgard archaea-related host being duplicated most. By relatively timing events using phylogenetic distances we inferred that duplications in cytoskeletal and membrane trafficking families were among the earliest events, whereas most other families expanded predominantly after mitochondrial endosymbiosis. Altogether, we infer that the host that engulfed the proto-mitochondrion had some eukaryote-like complexity, which drastically increased upon mitochondrial acquisition. This scenario bridges the signs of complexity observed in Asgard archaeal genomes to the proposed role of mitochondria in triggering eukaryogenesis.

From the discussion,

This large-scale analysis of duplications during eukaryogenesis provides compelling evidence for a mitochondria-intermediate eukaryogenesis scenario. The results suggest that the Asgard archaea-related host already had some eukaryote-like cellular complexity, such as a dynamic cytoskeleton and membrane trafficking. Upon mitochondrial acquisition there was an even further increase in complexity with the establishment of a complex signalling and transcription regulation network and by shaping the endomembrane system. These post-endosymbiosis innovations could have been facilitated by the excess of energy allegedly provided by the mitochondrion28,29.

A relatively complex host is in line with the presence of homologues of eukaryotic cytoskeletal and membrane trafficking genes in Asgard archaeal genomes5,6,30. Moreover, some of them, including ESCRT-III homologues, small GTPases and (loki)actins, have duplicated in these archaea as well, either before eukaryogenesis or more recently5,6,30. This indicates that there has already been a tendency for at least the cytoskeleton and membrane remodelling to become more complex in Asgard archaeal lineages. A dynamic cytoskeleton and trafficking system, perhaps enabling primitive phagocytosis31, might have been essential for the host to take up the bacterial symbiont. Molecular and cell biology research in these archaea, from which the first results have recently become public32,33, is highly promising to yield more insight into the nature of the host lineage. In addition to a reconstruction of the host, further exploration of the numerous acquisitions, inventions and duplications during eukaryogenesis is key to fully unravelling the origin of eukaryotes.

 

[lpetrich]

Formation of chimeric genes with essential functions at the origin of eukaryotes | BMC Biology | Full Text

Background

Eukaryotes evolved from the symbiotic association of at least two prokaryotic partners, and a good deal is known about the timings, mechanisms, and dynamics of these evolutionary steps. Recently, it was shown that a new class of nuclear genes, symbiogenetic genes (S-genes), was formed concomitant with endosymbiosis and the subsequent evolution of eukaryotic photosynthetic lineages. Understanding their origins and contributions to eukaryogenesis would provide insights into the ways in which cellular complexity has evolved.

Results

Here, we show that chimeric nuclear genes (S-genes), built from prokaryotic domains, are critical for explaining the leap forward in cellular complexity achieved during eukaryogenesis. A total of 282 S-gene families contributed solutions to many of the challenges faced by early eukaryotes, including enhancing the informational machinery, processing spliceosomal introns, tackling genotoxicity within the cell, and ensuring functional protein interactions in a larger, more compartmentalized cell. For hundreds of S-genes, we confirmed the origins of their components (bacterial, archaeal, or generally prokaryotic) by maximum likelihood phylogenies. Remarkably, Bacteria contributed nine-fold more S-genes than Archaea, including a two-fold greater contribution to informational functions. Therefore, there is an additional, large bacterial contribution to the evolution of eukaryotes, implying that fundamental eukaryotic properties do not strictly follow the traditional informational/operational divide for archaeal/bacterial contributions to eukaryogenesis.

Conclusion

This study demonstrates the extent and process through which prokaryotic fragments from bacterial and archaeal genes inherited during eukaryogenesis underly the creation of novel chimeric genes with important functions.

Chimeric genes: genes assembled from other genes.

 

[lpetrich]

Evidence for a Syncytial Origin of Eukaryotes from Ancestral State Reconstruction | Genome Biology and Evolution | Oxford Academic

Modern accounts of eukaryogenesis entail an endosymbiotic encounter between an archaeal host and a proteobacterial endosymbiont, with subsequent evolution giving rise to a unicell possessing a single nucleus and mitochondria. The mononucleate state of the last eukaryotic common ancestor (LECA) is seldom, if ever, questioned, even though cells harboring multiple (syncytia, coenocytes, and polykaryons) are surprisingly common across eukaryotic supergroups. Here, we present a survey of multinucleated forms. Ancestral character state reconstruction for representatives of 106 eukaryotic taxa using 16 different possible roots and supergroup sister relationships, indicate that LECA, in addition to being mitochondriate, sexual, and meiotic, was multinucleate. LECA exhibited closed mitosis, which is the rule for modern syncytial forms, shedding light on the mechanics of its chromosome segregation. A simple mathematical model shows that within LECA’s multinucleate cytosol, relationships among mitochondria and nuclei were neither one-to-one, nor one-to-many, but many-to-many, placing mitonuclear interactions and cytonuclear compatibility at the evolutionary base of eukaryotic cell origin. Within a syncytium, individual nuclei and individual mitochondria function as the initial lower-level evolutionary units of selection, as opposed to individual cells, during eukaryogenesis. Nuclei within a syncytium rescue each other’s lethal mutations, thereby postponing selection for viable nuclei and cytonuclear compatibility to the generation of spores, buffering transitional bottlenecks at eukaryogenesis. The prokaryote-to-eukaryote transition is traditionally thought to have left no intermediates, yet if eukaryogenesis proceeded via a syncytial common ancestor, intermediate forms have persisted to the present throughout the eukaryotic tree as syncytia but have so far gone unrecognized.

Multinucleate cells are very common across eukaryotedom.

•  Syncytium - from aggregation
•  Coenocyte - from nuclear division without separation into cells

There is also a difference between kinds of cell division:

• Open: nuclear membrane dissolves, then reforms around the two copies of chromosomes
• Closed: nuclear membrane stays in place, then splits for the two copies

Closed division is typical in multinucleate cells.

They counted as multinucleate all organisms with some multinucleate phase or body part. Phase? Some insects, like the lab fruit fly Drosophila melanogaster, go through an early-embryonic multinucleate phase. Body part? Animal muscles are often multinucleate. So they counted the *ability* to be multinucleate, even if it separately emerged several times.

Being multinucleate is widespread in eukaryotedom, and the best-known ones are multicellular fungi. Many amoebozoans are also multinucleate, as are many rhizarians and some alveolates. Photosynthetic eukaryotes are often multinucleate, like many green algae, red algae, and stramenopile algae.


I couldn't quite figure out how they counted polyploidy. Meiosis involves starting from a diploid phase, and a diploid cell that does ordinary reproduction (mitosis) goes through a tetraploid phase. Did they mean polyploidy like from diploid-phase mitosis?