The criterion of efficiency of mitochondria is taken as the yield of ATP per carbohydrate molecule oxidized using the electron transport chain and oxidative phosphorylation. Experimental values for this are similar for yeast and humans, whereas theoretical values derived from differences in the structures of the ATP synthases actually imply a higher yield for mammalian mitochondria.
It is argued that it is not surprising that the difference in generation times did not produce the result expected by the poster. First, the period after the separation of eukaryotes from prokaryotes is no longer than the period between the origin of eukaryotes and that of the aerobic bacteria from which their mitochondria arose. Second, the stage would have been reached when there were mechanistic limitations on further increases in efficiency of this complex system. If the differences between mammalian and yeast bacterial ATP synthases is real (and an even ‘worse’ yield for bacteria, that have an even shorter generation time), this suggests that the main evolutionary pressure on this system varies between organisms, rather than being simply to maximize the yield of ATP.
Criterion of efficiency
The main function of mitochondria is to use molecular oxygen to oxidize NADH and FADH2 via the electron transport chain and oxidative phosphorylation to produce ATP. A suitable and generally accepted measure of efficiency — reminiscent of that applied to man-made mechanical devices — would be the percentage of the energy of this oxidation that is converted to ATP (rather than being released as heat). Any reader not familiar with the biochemistry of this system is advised to read the footnote* before proceeding further.
Is there any difference?
The traditional way in which the yield of ATP in oxidative phosphorylation has been measured is by the P/O ratio (the ratio of ATP produced to oxygen consumed). Results obtained over the years have varied becauase of technical problems — see review by Hinkle (2005). As summarized more recently (2010) by SJ Ferguson, the historical controversy was not about differences between species — they were no indications of differences even between bacteria (the precursors of mitochondria, performing oxidative phosphorylation in their intermembrane space) — but merely about the true value of the P/O ratio.
As Ferguson goes on to say, the gradual elucidation of the structure of the ATP synthase and the elucidation of its mechanism led to a believe that deductions from this were a more reliable indication of the stoichiometry than the experimental measurements. Specifically, a 360˚ rotation of the F0 component of the ATP synthase could be seen to result in the synthesis of one molecule of ATP, and that this required on hydrogen ion bound to each of its c subunits (see diagram from Wikipedia article, below).
He describes the results with yeast as follows:
X-ray crystallography of yeast ATP synthase revealed a ring of c subunits attached to F1 even in the absence of other subunits of the F0 sector (9). This work not only suggested that a and b were not interdigitated with c but also revealed the surprising stoichiometry of c10. The C-terminal helix of the hairpin c subunit is at the outside of the ring and contains an essential aspartate or glutamate residue. This residue is believed to pick up an H+ and rotate away from an interaction with the α subunit. Thus, 10 protons should drive a 360° rotation of the c ring, which is structurally connected to γ, giving synthesis of 3 ATPs as γ rotates through 360° within F1; the H+/ATP ratio would be 10/3 = 3.3. The P/O ratio for NADH would be 10/(3.3 + 1) = 10/4.3 ≈ 2.3, thus moving below the range of values directly determined.
It was assumed that ATP synthases other than yeast would also have 10 c subunits, but, surprisingly, although bacterial ATP synthases also have 10 subunits, the bovine (and other vertebrate) one has only 8, suggesting a higher P/O ratio than yeast — greater, not poorer, efficiency.
Mitochondrial evolution in context
Whatever the actual P/O ratios in different aerobes, the more rapidly-dividing species do not show a clear increase in efficiency in this respect. I suggest that in this respect the evolutionary timescale shown below (adapted from The Cell: A Molecular Approach) should be considered.
What is clear is that the time for an improvement in efficiency of energy production to occur between the divergence of yeast and animals (A) is much less than that between the time at which mitochondria were acquired from bacteria by the first aerobic eukaryote (B–A). Note also the long period the system had to evolve in the aerobic bacterium that gave rise to mitochondria (C–B). My argument is that by the time of appearance of mitochondria, the system had time to evolve to the optimum that mechanistic considerations would allow. Otherwise one would have expected those bacteria to further evolve a system much superior to yeast or mammals in the C–B timescale.
Other aspects of the evolution of the mitochondrial energy generating system
It should be noted that there have been changes in the mitochondrial energy generating system over evolutionary time. For example, in the cytochrome oxidase system the same set of core subunits are found in prokaryotes and eukaryotes. However additional subunits have been acquired in primates. Rather than being concerned with the catalytic efficiency of the system, these additional subunits are thought to be concerned with regulation.
Better systems to study the effect of division time on evolution of eukaryotic ‘efficiency’?
Because mitochondria had probably reached optimal mechanistic efficiency in energy generation when they were acquired, they do not appear to be a good choice for studies of the type the poster envisages. Perhaps he might do better with something related to nuclei, which are not present in bacteria. However there are problems of interpretation. For example, if it were found that some aspect of the DNA replication machinery in yeast allowed this process to proceed faster than that in mammals, could one conclude that this was due to the shorter generation time of yeast? No! One could equally argue (and it would seem to me more likely) that the lower generation time resulted from an evolutionary pressure for faster DNA replication, a pressure that does not exist in the more slowly dividing mammals.
ATP in mitochondria (and the inner membrane of aerobic bacteria) is synthesized from ADP using the free energy released by the oxidation of the reduced cofactors, NADH and FADH2 (produced from the oxidation of particular carbohydrates), by molecular oxygen. The mechanism of this, rather than involving simple coupled chemical reactions, involves the movement of hydrogen ions across a membrane in which there is a concentration gradient (strictly through a proton motive force, to which membrane charge also contributes) using an ATP synthase, a molecular machine, the structure of which clearly indicates the stoichiometry of input hydrogen ions to ATP synthesized. The hydrogen ion gradient results from three stages in the electron transport chain (complexes I, III and IV) where a hydrogen ion is translocated into the inner mitochondrial intermembrane space. This is described in standard text books of biochemistry such as Berg et al..