File Name: origin and early evolution of the metazoa .zip
- History of life
- Origin and Early Evolution of the Metazoa
- The origin of Metazoa: a transition from temporal to spatial cell differentiation
History of life
Metrics details. Phylogenomics of eukaryote supergroups suggest a highly complex last common ancestor of eukaryotes and a key role of mitochondrial endosymbiosis in the origin of eukaryotes. The origin of eukaryotes is a huge enigma and a major challenge for evolutionary biology [ 1 — 3 ].
There is a sharp divide in the organizational complexity of the cell between eukaryotes, which have complex intracellular compartmentalization, and even the most sophisticated prokaryotes archaea and bacteria , which do not [ 4 — 6 ]. A typical eukaryotic cell is about 1,fold bigger by volume than a typical bacterium or archaeon, and functions under different physical principles: free diffusion has little role in eukaryotic cells, but is crucial in prokaryotes [ 7 , 8 ].
The compartmentalization of eukaryotic cells is supported by an elaborate endomembrane system and by the actin-tubulin-based cytoskeleton [ 9 , 10 ]. There are no direct counterparts of these organelles in archaea or bacteria. The other hallmark of the eukaryotic cell is the presence of mitochondria, which have a central role in energy transformation and perform many additional roles in eukaryotic cells, such as in signaling and cell death.
The conservation of the major features of cellular organization and the existence of a large set of genes that are conserved across eukaryotes leave no doubt that all extant eukaryotic forms evolved from a last eukaryote common ancestor LECA; see below. All eukaryotes that have been studied in sufficient detail possess either mitochondria or organelles derived from mitochondria [ 11 — 13 ], so it is thought that LECA already possessed mitochondria see below.
Plants and many unicellular eukaryotes also have another type of organelle, plastids. The organizational complexity of the eukaryotic cells is complemented by extremely sophisticated, cross-talking signaling networks [ 14 ]. The main signaling systems in eukaryotes are the kinase-phosphatase machinery that regulates protein function through phosphorylation and dephosphorylation [ 15 — 18 ]; the ubiquitin network that governs protein turnover and localization through reversible protein ubiquitylation [ 19 — 21 ]; regulation of translation by microRNAs [ 22 — 24 ]; and regulation of transcription at the levels of individual genes and chromatin remodeling [ 24 — 27 ].
Eukaryotes all share the main features of cellular architecture and the regulatory circuitry that clearly differentiate them from prokaryotes, although the ancestral forms of some signature eukaryotic systems are increasingly detected in prokaryotes, as discussed below. Phylogenomic reconstructions show that the characteristic eukaryotic complexity arose almost 'ready made', without any intermediate grades seen between the prokaryotic and eukaryotic levels of organization [ 9 , 28 — 30 ].
Explaining this apparent leap in complexity at the origin of eukaryotes is one of the principal challenges of evolutionary biology. The key to the origin of eukaryotes will undoubtedly be found using comparative genomics of eukaryotes, archaea and bacteria. Complete genome sequences from all three domains of cellular life are accumulating exponentially, albeit at markedly different paces.
As of March , the NCBI genome database contained over 1, bacterial genomes, about archaeal genomes, and about genomes of eukaryotes [ 31 ]. Here, I discuss some of the main insights that have come from comparative analysis of these genomes, which may help to shed light on the origin and the early stages of evolution of eukaryotes.
So far, the comparative genomics era has brought fascinating clues but no decisive breakthrough. Although several eukaryotic kingdoms, such as animals, fungi, plants and ciliates, are well defined and seem to be monophyletic beyond reasonable doubt, deciphering the evolutionary relationships between these kingdoms and numerous other groups of unicellular eukaryotes also called protists turned out to be daunting.
For many years, evolutionary biologists tended to favor the so called crown group phylogeny [ 2 , 32 ]. The 'crown' of this evolutionary tree included animals Metazoa and plants Viridiplantae , fungi and various assortments of protists, depending on the methods used for tree construction [ 33 , 34 ].
The rest of the protists, such as microsporidia, diplomonads and parabasalia, were considered 'early branching eukaryotes'; for some of them, this conclusion was reached because they appeared to lack mitochondria and were therefore thought to have evolved before the mitochondrial symbiosis. The scenario resulting from the crown group phylogeny was called the archezoan scenario: the archaezoan was defined as a hypothetical ancestral form that lacked mitochondria but possessed the other signature features of the eukaryotic cell.
However, during the past decade, the early branching groups have lost their positions at the root of the eukaryotic tree, one after another [ 35 — 37 ]. The improved taxon sampling as a result of genome sequencing together with new, more robust methods for phylogenetic analysis indicate that the deep placing of these groups seen in early trees was a long-branch artifact caused by the fast evolution of the respective organisms [ 37 — 39 ].
At the same time, comparative-genomic and ultrastructural studies destroyed the biological underpinning of the near-root positions of the former early branching groups of protists by showing that none of them ancestrally lack mitochondria, as they all have genes of apparent mitochondrial origin and mitochondria-related organelles, such as hydrogenosomes and mitosomes [ 11 , 12 , 13 , 40 ].
There are therefore no grounds to consider any group of eukaryotes primitive, a presymbiotic archezoan. Rather, taking into account the small genomes and high rate of evolution characteristic of most of the protist groups thought to be early branching, and their parasitic lifestyle, it is becoming increasingly clear that most or perhaps all of them evolved from more complex ancestral forms by reductive evolution [ 37 , 39 ].
Reductive evolution refers to the evolutionary modality typical of parasites: they tend to lose genes, organelles and functions when the respective functionalities are taken over by the host. So the archezoan crown group phylogeny seems to have been disproved, and deep phylogeny and the theories of the origin of eukaryotes effectively had to start from scratch.
This time phylogenomic approaches were mainly used, that is, phylogenetic analysis of genome-wide sets of conserved genes; this was made possible by the much larger number of genomes that had been sequenced [ 41 , 42 ]. The key accomplishment at this new stage was the proposal of 'supergroups' of eukaryotes that are suggested to combine highly diverse groups of organisms in a monophyletic group [ 36 , 43 — 45 ]. Most of the phylogenomic analyses published so far converge on five supergroups or six if the Amoebozoa and Opisthokonts do not form a single supergroup, the Unikonts; Figure 1.
Although proving monophyly is non-trivial for these groups [ 46 — 48 ], the general structure of the tree, with a few supergroups forming a star-like phylogeny Figure 1 , is reproduced consistently, and the latest results [ 49 — 52 ] seem to support the monophyly of the five supergroups.
Evolution of the eukaryotes. The relationship between the five eukaryotic supergroups - Excavates, Rhizaria, Unikonts, Chromalveolates and Plantae - are shown as a star phylogeny with LECA placed in the center. The 4, genes assigned to LECA are those shared by the free-living excavate amoeboflagellate Naegleria gruberi with representatives of at least one other supergroup [ 67 ]. The numbers of these putative ancestral genes retained in selected lineages from different supergroups are also indicated.
Branch lengths are arbitrary. Two putative root positions are shown: I, the Unikont-Bikont rooting [ 56 , 57 ]; II, rooting at the base of Plantae [ 60 ]. The relationship between the supergroups is a formidable problem as the internal branches are extremely short, suggesting that the radiation of the supergroups occurred rapidly on the evolutionary scale , perhaps resembling an evolutionary 'big bang' [ 53 — 55 ].
Two recent, independent phylogenetic studies [ 51 , 52 ] each analyzed over conserved proteins from several dozen eukaryotic species and, after exploring the effects of removing fast-evolving taxa, arrived at a three-megagroup structure of the eukaryotic tree.
The megagroups consist of Unikonts, Excavates, and the assemblage of Plantae, Chromalveolata and Rhizaria [ 51 , 52 ]. Furthermore, there have been several attempts to infer the position of the root of the eukaryotic tree Figure 1. The first alternative to the crown group tree was proposed by Cavalier-Smith and coworkers [ 56 — 58 ], who used rare genomic changes RGCs [ 59 ], such as the fusion of two enzyme genes [ 56 , 57 ] and the domain structure of myosins [ 58 ], to place the root between the Unikonts and the rest of eukaryotes I red arrow in Figure 1.
This separation seems biologically plausible because Unikont cells have a single cilium, whereas all other eukaryotic cells have two. However, this conclusion could be suspect because the use of only a few RGCs makes it difficult to rule out homoplasy parallel emergence of the same RGC, such as gene fusion or fission, in different lineages.
Rogozin and coworkers [ 60 ] used a different RGC approach based on rare replacements of highly conserved amino acid residues requiring two nucleotide substitutions and inferred the most likely position of the root to be between Plantae and the rest of eukaryotes II green arrow in Figure 1. Again, this seems biologically plausible because the cyanobacterial endosymbiosis that gave rise to plastids occurred on the Plantae lineage.
The controversy about the root position and the lack of consensus regarding the monophyly of at least some of the supergroups, let alone the megagroups, indicate that, despite the emerging clues, the deep phylogeny of eukaryotes currently should be considered unresolved. In a sense, given the likely 'big bang' of early eukaryote radiation, the branching order of the supergroups, in itself, might be viewed as relatively unimportant [ 61 ].
However, the biological events that triggered these early radiations are of major interest, so earnest attempts to resolve the deepest branches of the eukaryotic tree will undoubtedly continue with larger and further improved datasets and methods. Comparative analysis of representative genomes from different eukaryotic supergroups enables the reconstruction of the gene complement of LECA using maximum parsimony MP or more sophisticated maximum likelihood ML methods [ 62 — 64 ].
Essentially, genes that are represented in diverse extant representatives of different supergroups, even though lost in some lineages, can be mapped back to LECA. The results of all these reconstructions consistently point to a complex LECA, in terms of both the sheer number of ancestral genes and, perhaps even more importantly, the ancestral presence of the signature functional systems of the eukaryotic cell see below.
A MP reconstruction based on phyletic patterns in clusters of orthologous genes of eukaryotes mapped 4, genes to LECA Figure 1 [ 63 , 65 , 66 ]. Remarkably, an even simpler estimation, based on the recent analysis of the genome of Naegleria gruberi , the first sequenced genome of a free-living excavate [ 67 ], revealed about a nearly identical number of genes, 4,, that are shared by Naegleria and at least one other supergroup of eukaryotes, suggesting that these genes are part of the LECA heritage Figure 1.
Such estimates are highly conservative as they do not account for lineage-specific loss of ancestral genes, a major aspect in the evolution of eukaryotes. Given that the current estimate for the gene complement of LECA must be conservative, the genome of LECA is likely to have been as complex as those of typical extant free-living unicellular eukaryotes [ 68 ].
This conclusion is supported by reconstructions from comparative genomics of the ancestral composition of the key functional systems of the LECA, such as the nuclear pore [ 28 , 69 ], the spliceosome [ 29 ], the RNA interference machinery [ 70 ], the proteasome and the ubiquitin signaling system [ 71 ], and the endomembrane apparatus [ 10 ].
The outcomes of these reconstructions are all straightforward and consistent, even when different topologies of the phylogenetic tree of eukaryotes were used as the scaffold for the reconstruction: LECA already possessed all these structures in its fully functional state, possibly as complex as the counterparts in modern eukaryotes.
Reconstruction of other aspects of the genomic composition and architecture of LECA similarly points to a highly complex ancestral genome. Comparative-genomic analysis of intron positions in orthologous genes within and between supergroups suggests high intron densities in the ancestors of the supergroups and in LECA, at least as dense as in modern free-living unicellular eukaryotes [ 72 — 75 ].
A systematic analysis of widespread gene duplications in eukaryotes indicates that hundreds of duplications predate LECA, especially duplications of genes involved in protein turnover [ 63 , 65 , 66 ]. Taken together, these results clearly indicate that LECA was a typical, fully developed eukaryotic cell. The subsequent evolution of eukaryotes has seemingly shown no consistent trend toward increased complexity, except for lineage-specific embellishments, such as those seen in animals and plants.
There was obviously an important stage of evolution on the 'stem' of eukaryotes, after they first evolved but before LECA, which included extensive duplication of numerous essential genes, so that the set of ancestral genes approximately doubled [ 63 , 65 , 66 ].
Eukaryotes are hybrid organisms in terms of both their cellular organization and their gene complement. The gene complement of eukaryotes is an uneven mix of genes of apparent archaeal origin, genes of probable bacterial origin, and genes that so far seem eukaryote-specific, without convincing evidence of ancestry in either of the two prokaryote domains Figure 2.
Paradoxical as this might appear, although trees based on rRNA genes and concatenated alignments of information-processing proteins, such as polymerases or splicing proteins, both put archaea and eukaryotes together, genome-wide analyses consistently and independently show that there are three or more times more genes with bacterial homologs than with archaeal homologs [ 62 , 63 , 78 , 79 ] Figure 2.
The archaeal subset is strongly enriched in information processing functions translation, transcription, replication, splicing , whereas the bacterial subset consists largely of metabolic enzymes [ 62 , 78 ] see below for more details.
Breakdown of the genes from two eukaryotes by the putative evolutionary affinities. The putative origin of genes was tentatively inferred from the best hits obtained by searching the NCBI non-redundant protein sequence database using the BLASTP program [ ], with all protein sequences from the respective organisms used as queries.
Although sequence similarity searches are often regarded as a very rough approximation of the phylogenetic position [ ], the previous analysis of the yeast genome showed a high level of congruence between the best hits and phylogenomic results [ 78 ].
Major archaeal and bacterial groups are color-coded and denoted 1 to 18; the number of proteins with the best hit to the given groups is indicated. However, attempts to pinpoint the specific archaeal and bacterial 'parents' of eukaryotes reveal complicated evolutionary relationships. Apart from this uncertainty about the gene complement of the endosymbiont, it is impossible to rule out multiple sources of the bacterial-like genes in eukaryotes [ 83 ], which may have origins other than the genome of the bacterial endosymbiont.
In particular, whatever the actual nature of the archaeal-like ancestor, it probably lived at moderate temperatures and non-extreme conditions and was consequently in contact with a diverse bacterial community.
Modern archaea with such lifestyles have numerous genes of diverse bacterial origins, indicating extensive horizontal acquisition of genes from bacteria [ 84 , 85 ]. Thus, the archaeal-like host of the endosymbiont could have already had many bacterial genes, partly explaining the observed pattern. Phylogenomic studies using different methods point to different archaeal lineages - Crenarchaeota [ 86 , 87 ], Euryarchaeota [ 88 ], or an unidentified deep branch [ 89 , 90 ] - as the candidates for the eukaryote ancestor Figure 3.
Unequivocal resolution of such deep evolutionary relationships is extremely difficult. Moreover, at least one of these analyses [ 89 ] explicitly suggests the possibility that the archaeal heritage of eukaryotes is genuinely mixed, with the largest contribution coming from a deep lineage, followed by the contributions from Crenarchaeota Thaumoarchaeota and the Euryarchaeota Figure 3.
In the next section I examine the possibility of multiple archaeal and bacterial ancestors of the eukaryotes with respect to distinct functional systems of eukaryotic cells. Possible archaeal origins of eukaryotic genes. The archaeal tree is shown as a bifurcation of Euryarchaeota and the putative second major branch combining Crenarchaeota, Thaumarchaeota, and Korarchaeota [ ]; deep, possibly extinct lineages are shown as a single stem.
Some of the most compelling indications on the course of evolution and the nature of ancestral forms come from signature genes that are uniquely shared by two or more major lineages and from detailed evolutionary analysis of well characterized functional systems, in particular the signature systems of the eukaryotic cell.
Comparative genome sequence analysis has revealed that some of the key molecular machines of the eukaryotes, and not only those directly involved in information processing, can be confidently derived from archaeal ancestors Table 1 and Figure 4. Strikingly, this archaeal heritage seems to be patchy with respect to the specific origins, with apparent evolutionary affinities to different groups of archaea Table 1 and Figure 4. For instance, comparative analysis of the translation system components tends to suggest an affinity between eukaryotes and Crenarchaeota [ 91 ].
Similarly, the core transcription machinery of eukaryotes shares some important proteins with Crenarchaeota, Thaumarchaeota and Korarchaeota, to the exclusion of Euryarchaeota [ 92 — 94 ].
By contrast, the histones, the primary components of nucleosomes, are missing in most of the Crenarchaeota but invariably conserved in Euryarchaeota and also present in Korarchaeum and some Thaumarchaeota [ 95 ]. Apparent complex origins of some key functional systems of eukaryotes. The domains are not drawn to scale. Eukaryotic cell division components are also conserved in several but not all of the major archaeal lineages.
For example, homologs of the ESCRT-III complex, which performs key roles in vesicle biogenesis and cytokinesis in eukaryotes, are responsible for cell division in the Crenarchaeota but are missing in most of the Euryarchaeota, which possess a bacterial-like division mechanism using the GTPase FtsZ, a distant homolog of tubulin [ 96 , 97 ].
Origin and Early Evolution of the Metazoa
The theory of cellularization , also known as the syncytial theory or ciliate-acoel theory, is a theory to explain the origin of Metazoa. The cellularization theory states that metazoans evolved from a unicellular ciliate with multiple nuclei that went through cellularization. Firstly, the ciliate developed a ventral mouth for feeding and all nuclei moved to one side of the cell. Secondly, an epithelium was created by membranes forming barriers between the nuclei. In this way, a multicellular organism was created from one multinucleate cell syncytium. By several cellularization processes, the ciliate ancestor evolved into the currently known turbellarian flatworms , which are therefore the most primitive metazoans according to the theory.
Metrics details. The origin of animals from their unicellular ancestor was one of the most important events in evolutionary history, but the nature and the order of events leading up to the emergence of multicellular animals are still highly uncertain. The diversity and biology of unicellular relatives of animals have strongly informed our understanding of the transition from single-celled organisms to the multicellular Metazoa. Here, we analyze the cellular structures and complex life cycles of the novel unicellular holozoans Pigoraptor and Syssomonas Opisthokonta , and their implications for the origin of animals. Syssomonas and Pigoraptor are characterized by complex life cycles with a variety of cell types including flagellates, amoeboflagellates, amoeboid non-flagellar cells, and spherical cysts. The life cycles also include the formation of multicellular aggregations and syncytium-like structures, and an unusual diet for single-celled opisthokonts partial cell fusion and joint sucking of a large eukaryotic prey , all of which provide new insights into the origin of multicellularity in Metazoa. The feeding modes of the ancestral metazoan may have been more complex than previously thought, including not only bacterial prey, but also larger eukaryotic cells and organic structures.
PDF | A scenario for the evolutionary history of the Metazoa is presented, number of models for early metazoan evolution had been pro-.
The origin of Metazoa: a transition from temporal to spatial cell differentiation
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