When was the origin of eukaryotes

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This paper proposes a thorough systematic analysis of the phylogenetic relationships between ancestral eukaryotic genes and archaeal and bacterial genes. Ku, C. Endosymbiotic origin and differential loss of eukaryotic genes. Pittis, A. Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. This paper represents the first formal testing of the timing of acquisition of the mitochondrion by use of comparisons of phylogenetic distances between eukaryotic proteins and their closest prokaryotic relatives.

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The SAR11 group of alpha-proteobacteria is not related to the origin of mitochondria. Thrash, J. Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Brindefalk, B. A phylometagenomic exploration of oceanic alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. Wang, Z. An integrated phylogenomic approach toward pinpointing the origin of mitochondria.

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Among other topics, this review discusses the necessity to determine the mechanistic and selective forces explaining the origin of key eukaryotic features, such as the nucleus or the bacterial-like eukaryotic membrane system.

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The results of comparative genomics and ultrastructural studies do not yet definitively show where the eukaryotic cell came from, but they do offer important insights. Box 1 lists the key observations that must be included in any evolutionary scenario for the evolution of eukaryotes called eukaryogenesis and summarizes the two alternative scenarios, which are depicted in Figure 5.

The main issue revolves around the role of endosymbiosis [ 2 , 3 , , ]: was it the cause of the entire chain of events that led to the emergence of LECA the stem phase of evolution , as proposed by the symbiogenesis scenario, or was it a step in the evolution of the already formed eukaryotic cell, as proposed by the archaezoan scenario?

The two alternative scenarios of eukaryogenesis. Given that eukaryogenesis may have been a unique event and that intermediate stages in the process cannot be seen, these questions are enormously difficult, and final answers might not be attainable.

But the symbiogenesis scenario seems to be more plausible than the archaezoan scenario [ ], for three main reasons. First, under the archaezoan scenario, there is no plausible selective force behind the evolution of the nucleus, and in particular the elaborate nuclear pore complex.

The nucleus disrupts the transcription-translation coupling that is typical of bacteria and archaea [ — ] and necessitates the evolution of the time- and energy-consuming mechanism of nucleocytosolic transport of mRNA. At least some additional innovations of eukaryogenesis, such as the evolution of the nonsense-mediated decay of transcripts containing premature stop codons and expansion of the ubiquitin system, can be envisaged as part of the same chain of adaptations to the intron bombardment as the origin of the nucleus [ ] Figure 5.

Second, functional studies in prokaryotes, particularly archaea, show that not only the molecular components of the several signature eukaryotic systems but also their actual structures and functions have evolved in archaea and thus predate eukaryogenesis.

These include the archaeal proteasome [ ], exosome [ ] and Sm-protein complex, the progenitor of the spliceosome [ ], the ESCRT-III membrane remodeling system [ , ], actin-like proteins [ ] and a prototype of the ubiquitin system of protein modification [ ]. Each of these molecular machines found in different groups of archaea has been shown or predicted to be mechanistically similar to the eukaryotic counterpart, but they all function within the prokaryotic cell.

The endomembrane system and the nucleus are dramatic exceptions, and so are the mitochondria themselves. It is tempting to connect these dots by proposing that eukaryogenesis was triggered by endosymbiosis, and that the endomembrane systems including the nucleus evolved as defense against invasion of Group II introns and perhaps foreign DNA in general [ , ]. It does not seem accidental that many key components of these endomembrane systems seem to be of bacterial origin whereas others are repetitive proteins that might have evolved de novo [ 28 ].

Under the symbiogenesis scenario, diverse pre-existing systems of the archaeal host were co-opted and expanded within the emerging eukaryotic cellular organization [ 66 ]. Several arguments can be and have been put forward against the symbiogenesis scenario.

First, prokaryotic endosymbionts in prokaryotic hosts are not widespread, prompting the view that phagocytosis, which is apparently unique to eukaryotic cells, was critical for the acquisition of the mitochondrion [ 3 ]. This argument is not compelling because: 1 eukaryogenesis is extremely rare, probably unique, in the history of life; 2 endosymbiotic bacteria within other bacteria are rare but known [ — ], and intracellular bacterial predation has been suggested as a potential route to endosymbiosis [ ]; and 3 recent observations on membrane remodeling systems and actin-like proteins in archaea suggest the possibility of still unexplored mechanisms for engulfment of other prokaryotes, perhaps resembling primitive phagocytosis [ ].

Second, a potentially strong argument against the symbiogenesis scenario could be the existence of a substantial number of eukaryote signature proteins ESPs , so far found only in eukaryotes [ ]. The provenance of ESPs is an intriguing question. Under the symbiogenesis scenario, the former and remaining ESPs result primarily from acceleration of evolution of genes whose functions have substantially changed during eukaryogenesis.

However, the pangenomes of prokaryotes are large whereas the gene composition of individual organisms is highly flexible [ , ], so reconstruction of the actual partners of the endosymbiosis that led to eukaryogenesis might not be feasible from a limited set of extant genomes. Moreover, many if not most archaea and bacteria might have evolved by streamlining, so eukaryogenesis could have been triggered by symbiosis between two prokaryotes with complex genomes.

In short, it is currently impossible to strictly rule out the possibility that the key eukaryotic innovations evolved independently from and prior to the mitochondrial endosymbiosis.

In other words, the host of the endosymbiont might have been an archaezoan. In contrast, the symbiogenesis scenario can tie all these diverse lines of evidence into a coherent, even if still woefully incomplete, narrative.

Comparative genomics has so far neither solved the enigma of eukaryogenesis nor offered a definitive picture of the primary radiation of the major eukaryote lineages. However, although falling short of decisive answers, phylogenomic analysis has yielded many insights into the origin and earliest stages of evolution of eukaryotes.

Recent findings indicate that several key cellular systems of eukaryotes exist in archaea. The scattering of these systems among different archaeal lineages, along with the phylogenies of conserved proteins, suggests that the archaeal ancestor of eukaryotes belonged to a deep, possibly extinct archaeal branch with a highly complex genome and diverse cellular functionalities.

In contrast, the endomembrane systems of eukaryotes, and in particular the nucleus with its elaborate nuclear pore complex, are not found in archaea, and seem to be derived, at least in part, from bacterial ancestral components.

Phylogenomic analysis has clarified the evolutionary links between major groups of eukaryotes and led to the delineation of five or six supergroups. The relationships between the supergroups and the root position in the tree of eukaryotes remain extremely difficult to decipher, probably owing to a compressed cladogenesis or 'big bang' phase of evolution that followed eukaryogenesis.

The expanding sampling of genomes from diverse branches of life is far from being a trivial pursuit, but has rather delivered unexpected biological insights. Ovadi J, Saks V: On the origin of intracellular compartmentation and organized metabolic systems. Mol Cell Biochem.

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PLoS Biol. Genome Biol. Nucleic Acids Res. This hypothesis was also proposed and championed with the first direct evidence by Lynn Margulis. We now know that plastids are derived from cyanobacteria that lived inside the cells of an ancestral, aerobic, heterotrophic eukaryote.

This is called primary endosymbiosis, and plastids of primary origin are surrounded by two membranes. However, the best evidence is that the acquisition of cyanobacterial endosymbionts has happened twice in the history of eukaryotes. Almost all photosynthetic eukaryotes are descended from the first event, and only a couple of species are derived from the other, which in evolutionary terms, appears to be more recent. Cyanobacteria are a group of Gram-negative bacteria with all the conventional structures of the group.

However, unlike most prokaryotes, they have extensive, internal membrane-bound sacs called thylakoids. Chlorophyll is a component of these membranes, as are many of the proteins of the light reactions of photosynthesis. Cyanobacteria also have the peptidoglycan wall and lipopolysaccharide layer associated with Gram-negative bacteria. Chloroplasts of primary endosymbiotic origin have thylakoids, a circular DNA chromosome, and ribosomes similar to those of cyanobacteria.

As in mitochondria, each chloroplast is surrounded by two membranes. The outer membrane is thought to be derived from the enclosing vacuole of the host, and the inner membrane is thought to be derived from the plasma membrane of the cyanobacterial endosymbiont. In the group of Archaeplastida called the glaucophytes and in the rhizarian Paulinella , a thin peptidoglycan layer is still present between the outer and inner plastid membranes.

All other plastids lack this relict of the cyanobacterial wall. There is also, as with the case of mitochondria, strong evidence that many of the genes of the endosymbiont were transferred to the nucleus. Plastids, like mitochondria, cannot live independently outside the host. In addition, like mitochondria, plastids are derived from the division of other plastids and never built from scratch.

Researchers have suggested that the endosymbiotic event that led to Archaeplastida occurred 1 to 1. Not all plastids in eukaryotes are derived directly from primary endosymbiosis. Some of the major groups of algae became photosynthetic by secondary endosymbiosis, that is, by taking in either green algae or red algae both from Archaeplastida as endosymbionts Figure.

Numerous microscopic and genetic studies have supported this conclusion. Secondary plastids are surrounded by three or more membranes, and some secondary plastids even have clear remnants of the nucleus nucleomorphs of endosymbiotic algae. There are even cases where tertiary or higher-order endosymbiotic events are the best explanations for the features of some eukaryotic plastids. Visual Connection The Endosymbiotic Theory.

The first eukaryote may have originated from an ancestral prokaryote that had undergone membrane proliferation, compartmentalization of cellular function into a nucleus, lysosomes, and an endoplasmic reticulum , and the establishment of endosymbiotic relationships with an aerobic prokaryote, and, in some cases, a photosynthetic prokaryote, to form mitochondria and chloroplasts, respectively.

What evidence is there that mitochondria were incorporated into the ancestral eukaryotic cell before chloroplasts? The chloroplasts of red and green algae, for instance, are derived from the engulfment of a photosynthetic cyanobacterium by an ancestral prokaryote. This evidence suggests the possibility that an ancestral cell already containing a photosynthetic endosymbiont was engulfed by another eukaryote cell, resulting in a secondary endosymbiosis. Molecular and morphological evidence suggest that the chlorarachniophyte protists are derived from a secondary endosymbiotic event.

Chlorarachniophytes are rare algae indigenous to tropical seas and sand. They are classified into the Rhizarian supergroup. Chlorarachniophytes are reticulose amoebae, extending thin cytoplasmic strands that interconnect them with other chlorarachniophytes in a cytoplasmic network. These protists are thought to have originated when a eukaryote engulfed a green alga, the latter of which had previously established an endosymbiotic relationship with a photosynthetic cyanobacterium Figure.

Several lines of evidence support that chlorarachniophytes evolved from secondary endosymbiosis. The chloroplasts contained within the green algal endosymbionts still are capable of photosynthesis, making chlorarachniophytes photosynthetic. The green algal endosymbiont also exhibits a vestigial nucleus. In fact, it appears that chlorarachniophytes are the products of an evolutionarily recent secondary endosymbiotic event.

The plastids of chlorarachniophytes are surrounded by four membranes : The first two correspond to the inner and outer membranes of the photosynthetic cyanobacterium, the third corresponds to plasma membrane of the green alga, and the fourth corresponds to the vacuole that surrounded the green alga when it was engulfed by the chlorarachniophyte ancestor.

In other lineages that involved secondary endosymbiosis, only three membranes can be identified around plastids. This is currently interpreted as a sequential loss of a membrane during the course of evolution.

The process of secondary endosymbiosis is not unique to chlorarachniophytes. Secondary plastids are also found in the Excavates and the Chromalveolates. In the Excavates, secondary endosymbiosis of green algae led to euglenid protists, while in the Chromalveolates, secondary endosymbiosis of red algae led to the evolution of plastids in dinoflagellates, apicomplexans, and stramenopiles. The oldest fossil evidence of eukaryotes is about 2 billion years old. Fossils older than this all appear to be prokaryotes.

Its chromosomes were linear and contained DNA associated with histones. The nuclear genome seems to be descended from an archaean ancestor. This ancestor would have had a cytoskeleton and divided its chromosomes mitotically. It was aerobic because it had mitochondria derived from an aerobic alpha-proteobacterium that lived inside a host cell. Whether this host had a nucleus at the time of the initial symbiosis remains unknown.

The last common ancestor may have had a cell wall for at least part of its life cycle, but more data are needed to confirm this hypothesis. Figure What evidence is there that mitochondria were incorporated into the ancestral eukaryotic cell before chloroplasts?

Figure All eukaryotic cells have mitochondria, but not all eukaryotic cells have chloroplasts. Which of these protists is believed to have evolved following a secondary endosymbiosis? In , scientists published the genome of Monocercomonoides , and demonstrated that this organism has no detectable mitochondrial genes.

However, its genome was arranged in linear chromosomes wrapped around histones which are contained within the nucleus.

Which of the following observations about a bacterium would distinguish it from the last eukaryotic common ancestor? Eukaryotic cells arose through endosymbiotic events that gave rise to the energy-producing organelles within the eukaryotic cells such as mitochondria and chloroplasts. The nuclear genome of eukaryotes is related most closely to the Archaea, so it may have been an early archaean that engulfed a bacterial cell that evolved into a mitochondrion.

Mitochondria appear to have originated from an alpha-proteobacterium, whereas chloroplasts originated as a cyanobacterium. There is also evidence of secondary endosymbiotic events. Other cell components may also have resulted from endosymbiotic events.