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. 2020 Apr 28;15(1):8.
doi: 10.1186/s13062-020-00260-9.

Division of labour in a matrix, rather than phagocytosis or endosymbiosis, as a route for the origin of eukaryotic cells

Andrew Bateman  1   2
Affiliations

Division of labour in a matrix, rather than phagocytosis or endosymbiosis, as a route for the origin of eukaryotic cells

Andrew Bateman. Biol Direct. .

Abstract

Two apparently irreconcilable models dominate research into the origin of eukaryotes. In one model, amitochondrial proto-eukaryotes emerged autogenously from the last universal common ancestor of all cells. Proto-eukaryotes subsequently acquired mitochondrial progenitors by the phagocytic capture of bacteria. In the second model, two prokaryotes, probably an archaeon and a bacterial cell, engaged in prokaryotic endosymbiosis, with the species resident within the host becoming the mitochondrial progenitor. Both models have limitations. A search was therefore undertaken for alternative routes towards the origin of eukaryotic cells. The question was addressed by considering classes of potential pathways from prokaryotic to eukaryotic cells based on considerations of cellular topology. Among the solutions identified, one, called here the "third-space model", has not been widely explored. A version is presented in which an extracellular space (the third-space), serves as a proxy cytoplasm for mixed populations of archaea and bacteria to "merge" as a transitionary complex without obligatory endosymbiosis or phagocytosis and to form a precursor cell. Incipient nuclei and mitochondria diverge by division of labour. The third-space model can accommodate the reorganization of prokaryote-like genomes to a more eukaryote-like genome structure. Nuclei with multiple chromosomes and mitosis emerge as a natural feature of the model. The model is compatible with the loss of archaeal lipid biochemistry while retaining archaeal genes and provides a route for the development of membranous organelles such as the Golgi apparatus and endoplasmic reticulum. Advantages, limitations and variations of the "third-space" models are discussed. REVIEWERS: This article was reviewed by Damien Devos, Buzz Baum and Michael Gray.

Keywords: Archaea; Bacteria; Biofilm; Chromosomes; Eukaryogenesis; Eukaryotes; Evolution; Hypothesis; Matrix; Membranes; Mitochondria; Prokaryotes.

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Conflict of interest statement

The author declares that he has no competing interests.

Figures

Fig. 1
Fig. 1
Prokaryotic origins of eukaryotic genes. (A) The phylogenetic distribution of gene clades from a proposed model of the Last Eukaryotic Common Ancestor (LECA). The data was taken from [13] in which 434 LECA clades were identified. Of these 67 were of “uncertain” origin in which Archaea and Bacteria appeared mixed, 121 were of archaeal origin, and 234 of bacterial origin. Among the bacterial clades, 41 were clearly alpha-proteobacterial (from the proposed precursors for mitochondria), but the majority of the bacterial signal (labelled “non-defined”), while definitively bacterial, could not be confidently assigned to a phylum. The total bacterial columns (bact) is the sum of alpha-proteobacterial and non-defined bacterial clades. Trees were generated for eukaryotic, bacterial and archaeal gene families. These were then analyzed in terms of “configurations”, for example, those that branched cleanly between eukaryote and bacteria, were assigned as bacterial clades, etc. Only 3 clades (labelled bact/arch) have the so-called “three domain configuration”, that branched between Archaea, Bacteria, and Eukarya with no obvious bias between the three domains. (B). The proposed prokaryotic origins of genes in two extant organisms, a yeast (Saccharomyces cerevisiae, blue bars) and a red alga (Cyanidioschyzon merolae, orange bars) are compared. The data was taken from [8], and redrawn to eliminate the contribution from cyanobacteria since, in red algae, many of these genes would have been acquired subsequent to eukaryogenesis. A data point has been added to include the genetic contribution ascribed to all proteobacteria combined, (alpha, beta, gamma, delta/epsilon and unclassified proteobacteria). Approximately 60% of eukaryotic genes are attributed to an origin among prokaryotic sources; of these approximately 10% have an archaeal background (red arrows) and 50% have a bacterial background. Note that, as in panel (A), bacterial sources outnumber archaeal sources, and that the genes derived from alpha-proteobacteria (green arrow), show no evidence of over-representation. C-T-N stands for Crenarchaeota-Thaumarchaeota-Nanoarchaeota
Fig. 2
Fig. 2
Three potential pathways from prokaryotes to eukaryotes. In (a) two unipartite spaces fuse to form a bipartitite space that develops into a tripartitite eukaryotic progenitor [1* + 1*➔ 2*➔ 3*]. The initial unipartite spaces represented here are either a non-nucleated autogenously-derived proto-eukaryote and a bacterial space, or an archaeal space and bacterial space. The bacterial space is assumed to be the progenitor of the mitochondrial space (m), and fusion of the partner genomes is assumed to give rise to the nuclear space (N). In (b) a bipartite space, assumed here to be an autogenously-derived nucleated protoeukaryote, merges with a unipartite space, assumed here to be bacterial rather than archaeal, [2* + 1* ➔ 3*] to generate a eukaryotic progenitor cell. In (c), three unipartite spaces merge to give a tripartite space, [1* + 1* + 1* ➔ 3*]. In this manuscript the three spaces are assumed to be an archaeal space, a bacterial space and a matrix or third-space. The matrix serves as a proxy-cytoplasm, the two cellular spaces both contribute to the nucleus
Fig. 3
Fig. 3
Cell-like emergence from a matrix ensemble. a A consortium of cells in a matrix propagates by matrix dissolution to release cells as a unicellular planktonic phase cells that disperses and may reform a biofilm. b A stable matrix/cell ensemble undergoes progressive transitions towards an autonomous cell-like life style. Either the entire ensemble evolves into a cell-like life form (upper pathway), or subsets of cells within the ensemble matrix progressively become sufficiently autonomous to survive without the support of the matrix (breakout, lower pathway)
Fig. 4
Fig. 4
A brief outline of steps from prokaryotic cells in a matrix to a progenitor eukaryotic cell. a A transient consortium of prokaryotic cells (red Archaea, blue bacteria) in a biofilm-like or matrix undergoes a transformation to a stable ensemble of cells that encourages gene transfer resulting in increasingly hybridized genomes. Physical merger of cells results in multigenomes, with division of labour resulting in differentiation into mitochondria and nucleus. b In the yellow stream, a primitive nucleus emerges from a population of prokaryotic cells in a stable matrix through a succession of gene transfers resulting in merged genomes followed by cell fusions to result in multi-genome structures with multiple non-identical chromosomes. The genetic redundancy of the process supports the evolution of complex molecular pathways. b In the blue stream, developing interdependence among cells in a stable matrix allows for the emergence of increasingly elaborate protein networks that are supported by matrix-based (and ultimately cytoplasmic) ribosomes. In the green stream, as the population becomes progressively interdependent some cells in the matrix become ATP secretors, supplementing the energy needs of other cells and ultimately evolving into primitive mitochondria. Please consult the main text for more information
Fig. 5
Fig. 5
A comparison of autogenous and prokaryotic endosymbiotic models of eukaryogenesis with third-space model. In the autogenesis model, Proto-eukaryotes, Archaea and Bacteria all emerge from a last universal common ancestor. The Proto-eukaryotes then acquire a bacterial mitochondrial precursor by phagocytosis. In prokaryotic endosymbiosis, only Archaea and Bacteria connect directly to a last universal ancestor. Eukaryotes emerge as the result of endosymbiosis of an archaeon (the host) with a eubacterium (the passenger) that subsequently evolves into the eukaryotic mitochondrion. Massive horizontal gene transfer (H.G.T) then transfers the majority of prokaryote-derived genes to the emerging eukaryote. In the strong third-space model only Archaea and Bacteria link directly to a last universal ancestor. By co-existing in a closed and stable third-space, mitochondria and nuclei emerge by division of labour, gene transfer and cell fusion
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