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. 2011 Jun 30;6:35.
doi: 10.1186/1745-6150-6-35.

Energetics and Genetics Across the Prokaryote-Eukaryote Divide

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Free PMC article

Energetics and Genetics Across the Prokaryote-Eukaryote Divide

Nick Lane. Biol Direct. .
Free PMC article

Abstract

Background: All complex life on Earth is eukaryotic. All eukaryotic cells share a common ancestor that arose just once in four billion years of evolution. Prokaryotes show no tendency to evolve greater morphological complexity, despite their metabolic virtuosity. Here I argue that the eukaryotic cell originated in a unique prokaryotic endosymbiosis, a singular event that transformed the selection pressures acting on both host and endosymbiont.

Results: The reductive evolution and specialisation of endosymbionts to mitochondria resulted in an extreme genomic asymmetry, in which the residual mitochondrial genomes enabled the expansion of bioenergetic membranes over several orders of magnitude, overcoming the energetic constraints on prokaryotic genome size, and permitting the host cell genome to expand (in principle) over 200,000-fold. This energetic transformation was permissive, not prescriptive; I suggest that the actual increase in early eukaryotic genome size was driven by a heavy early bombardment of genes and introns from the endosymbiont to the host cell, producing a high mutation rate. Unlike prokaryotes, with lower mutation rates and heavy selection pressure to lose genes, early eukaryotes without genome-size limitations could mask mutations by cell fusion and genome duplication, as in allopolyploidy, giving rise to a proto-sexual cell cycle. The side effect was that a large number of shared eukaryotic basal traits accumulated in the same population, a sexual eukaryotic common ancestor, radically different to any known prokaryote.

Conclusions: The combination of massive bioenergetic expansion, release from genome-size constraints, and high mutation rate favoured a protosexual cell cycle and the accumulation of eukaryotic traits. These factors explain the unique origin of eukaryotes, the absence of true evolutionary intermediates, and the evolution of sex in eukaryotes but not prokaryotes.

Reviewers: This article was reviewed by: Eugene Koonin, William Martin, Ford Doolittle and Mark van der Giezen. For complete reports see the Reviewers' Comments section.

Figures

Figure 1
Figure 1
Genomes and membranes in eukaryotes and prokaryotes. (a). TEM of cyanobacteria, showing large expansion of bioenergetic membrane surface area as internal thylakoid membranes. However, cyanobacteria are sufficiently small that one or a few copies of the genome (not visible) are sufficient to retain control over chemiosmotic coupling. Scale bars: 50 nm. Reproduced with permission from Miller SR et al. PNAS 2005, 102:850-855. (b). TEM of intracellular bacteria living within free-living cyanobacteria (Pleurocapsa minor): one of only two known examples of a prokaryote inside a (walled) prokaryote, which must have gained entry without phagocytosis. Scale bars: 1 μM. Reproduced with permission from Wujek D. Trans Am Micros Soc 1979, 98:143-145. (c). Multiple copies of nucleoids, each containing the complete genome of Thiomargarita, stained with DAPI. Giant vacuole above in black. Scale bar 50 μM. Courtesy of Heide Schultz-Vogt. (d). Extreme polyploidy in Epulopiscium, (stained with DAPI) showing peri-membrane location of nucleoids, each genome about 3.8 Mb in size. Scale bar 50 μM. Courtesy of Esther Angert.
Figure 2
Figure 2
Endosymbiotic origin of eukaryotes by time and genetic distance. Schematic depiction of the chimeric origin of eukaryotes (in red) by (a) genetic distance and (b) time. Bacteria and archaea are shown to the left and right, respectively. Reticular networks of lateral gene transfer are not shown for simplicity, but characterise prokaryotic evolution. In (a) the unbranching red trunk depicts the prokaryote-eukaryote transition without any successful speciation (as attested by the absence of true evolutionary intermediates; see text) across the long genetic distance from an endosymbiotic origin in prokaryotes to LECA. In (b) the absence of this unbranching trunk depicts the short timescale and rapid evolution of LECA, driven by endosymbiotic gene transfer, a high mutation rate, cell fusions and genome doublings, accumulating traits within a single small population.
Figure 3
Figure 3
Energetics of genome size in eukaryotes and prokaryotes. (a). Mean energy per gene in prokaryotes versus eukaryotes equalised for genome size. Prokaryotes in red, eukaryotes in blue. Note log scale. (b). Mean energy per gene in prokaryotes versus eukaryotes equalised for genome size and cell volume; see text. Prokaryotes in red, eukaryotes in blue. Note log scale. (c). Power per haploid genome (energy per gene x number of genes in one haploid genome) in a. E. coli (metabolic rate taken from Ref 60); b. Thiomargarita (metabolic rate taken from Ref 83); c. Epulopiscium (metabolic rate taken, conservatively, to be equal to A. proteus); d. Chlamydomonas (metabolic rate taken from Ref 60); e. Amoeba proteus (metabolic rate taken from Ref 61). Note log scale and broad agreement with derived mean values in (a) and (b). (d). Proportion of genome free to vary (in red) equalised to 100,000 Mb in a. Epulopiscium and b. Amoeba proteus. Blue bar depicts proportion of total DNA content required for maintaining control over cytoplasm using an equal copy number (26,000; scaled from values given in text) of a. a 3.8 Mb genome; and b. a 30 Kb mitochondrial genome. 'Free to evolve' means genomic capacity beyond a standard prokaryotic genome required to govern a fixed volume of cytoplasm.
Figure 4
Figure 4
Volume of cytoplasm controlled by a single genome. The long reach of the eukaryotic gene. Mean eukaryotic cell volume is 15,000 times greater than mean bacterial cell volume (red circle), and is controlled by a single nuclear genome. In the case of Thiomargarita (yellow circle) the cell volume is larger than most eukaryotic cells but is mostly filled with inert vacuole. The band of active cytoplasm contains multiple nucleoids, each one governing a volume of cytoplasm equivalent to a single E. coli cell, hence volume per gene is prokaryotic.

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