Bioenergetic constraints on the evolution of complex life

Abstract

All morphologically complex life on Earth, beyond the level of cyanobacteria, is eukaryotic. All eukaryotes share a common ancestor that was already a complex cell. Despite their biochemical virtuosity, prokaryotes show little tendency to evolve eukaryotic traits or large genomes. Here I argue that prokaryotes are constrained by their membrane bioenergetics, for fundamental reasons relating to the origin of life. Eukaryotes arose in a rare endosymbiosis between two prokaryotes, which broke the energetic constraints on prokaryotes and gave rise to mitochondria. Loss of almost all mitochondrial genes produced an extreme genomic asymmetry, in which tiny mitochondrial genomes support, energetically, a massive nuclear genome, giving eukaryotes three to five orders of magnitude more energy per gene than prokaryotes. The requirement for endosymbiosis radically altered selection on eukaryotes, potentially explaining the evolution of unique traits, including the nucleus, sex, two sexes, speciation, and aging.

Figure 1.

Proposed vectorial reduction of CO₂ by H₂ across a thin FeS barrier. The reduction potential (E_h) of the H⁺/H₂ couple is –590 mV at pH 10, whereas the E_h of the CO₂/HCOOH couple at pH 6 is –370 mV, and the E_h of the HCOOH/CH₂O is –520 mV. A semiconducting FeS barrier should “feel” the distinct reduction potentials in both compartments and transfer electrons from H₂ to CO₂, to produce simple organics such as formaldehyde (CH₂O).

Figure 2.

Energetics of genome size in eukaryotes and prokaryotes. (A) Mean energy per gene in prokaryotes versus eukaryotes equalized for genome size. (Gray) Prokaryotes; (black) eukaryotes. Note the log scale. (B) Mean energy per gene in prokaryotes versus eukaryotes equalized for genome size and cell volume (see text). (Gray) Prokaryotes; (black) eukaryotes. Note the log scale. (C) Mean energy per gram in prokaryotes versus eukaryotes. (D) Power per haploid genome (energy per gene × number of genes in one haploid genome) in (lane a) Escherichia coli; (lane b) Thiomargarita; (lane c) Epulopiscium; (lane d) Chlamydomonas; and (lane e) Amoeba proteus. Note the log scale and broad agreement with derived mean values in A and B. (Figure based on data from Lane 2011a.)

Figure 3.

Size and morphological complexity of eukaryotic alga versus cyanobacterium. Approximately scaled comparison of (A) the eukaryotic alga Euglena with (B) the relatively large complex cyanobacterium Synechocystis, here approximately to scale. Despite its extensive internal thylakoid membranes (magnified in C) and moderate polyploidy (100–200 copies of nucleoid), Synechocystis is approximately 1500 times smaller by volume. (Courtesy of Mark Farmer, University of Georgia.)

Figure 4.

The apoptotic threshold is variable and determines fitness. The threshold for apoptosis can be raised or lowered in principle (center panel). If the threshold is low (left) even a small increase in free-radical leak triggers apoptosis. A low tolerance for free-radical leaks selects for good mitonuclear coadaptation, with predicted costs and benefits listed in the left-hand panel, correspondingly to a K reproductive strategy. High tolerance for free-radical leaks raises the threshold for apoptosis. This relaxes selection for mitonuclear coadaptation, corresponding to an r reproductive strategy, with the costs and benefits listed in the right-hand panel.