Membranes, energetics, and evolution across the prokaryote-eukaryote divide

Abstract

The evolution of the eukaryotic cell marked a profound moment in Earth's history, with most of the visible biota coming to rely on intracellular membrane-bound organelles. It has been suggested that this evolutionary transition was critically dependent on the movement of ATP synthesis from the cell surface to mitochondrial membranes and the resultant boost to the energetic capacity of eukaryotic cells. However, contrary to this hypothesis, numerous lines of evidence suggest that eukaryotes are no more bioenergetically efficient than prokaryotes. Thus, although the origin of the mitochondrion was a key event in evolutionary history, there is no reason to think membrane bioenergetics played a direct, causal role in the transition from prokaryotes to eukaryotes and the subsequent explosive diversification of cellular and organismal complexity.

Keywords: B. subtilis; E. coli; bioenergetics; cellullar evolution; evolutionary biology; genomics; human; lipids; mitochondrion; mouse.

Figure 1.. Scaling features of membrane properties with cell size.

(a) Relationship between the total outer surface area of mitochondria and that of the plasma membrane for all species with available data. Diagonal lines denote three idealized ratios of the two. (b) The number of ATP synthase complexes per cell scales with cell surface area (S, in μm²) as $113S^{1.26}$ ($r^2=0.99$). (c) Relationship between the total (inner + outer) surface area of mitochondria and cell volume for all species with available data. Open points are extrapolations for species with only outer membrane measures, derived by assuming an inner:outer ratio of 4.6, the average of observations in other species. References to individual data points are provided in Appendix 1–tables 1 and 2.

Figure 2.. The number of ribosomes per cell scales with cell volume (V, in μm³) as 7586V^0.82 (r² = 0.92; SEs of the intercept and slope on the log scale are 0.13 and 0.05, respectively).

Color coding as in previous figures. The data presented in this figure can be found in Figure 2—source data 1; see also Appendix 1–table 3.

Appendix 1—figure 1.. Relative contribution of ATP (P) and NADH/NADPH/FADH2 (H) to the biosynthetic costs of lipids and amino acids.

(A) Nonreduced costs including opportunity cost of precursors; (B) Reduced costs without precursors. Amino acid values are obtained from Akashi and Gojobori (2002), assuming growth on glucose.