Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template

Abstract

Oxidative phosphorylation couples ATP synthesis to respiratory electron transport. In eukaryotes, this coupling occurs in mitochondria, which carry DNA. Respiratory electron transport in the presence of molecular oxygen generates free radicals, reactive oxygen species (ROS), which are mutagenic. In animals, mutational damage to mitochondrial DNA therefore accumulates within the lifespan of the individual. Fertilization generally requires motility of one gamete, and motility requires ATP. It has been proposed that oxidative phosphorylation is nevertheless absent in the special case of quiescent, template mitochondria, that these remain sequestered in oocytes and female germ lines and that oocyte mitochondrial DNA is thus protected from damage, but evidence to support that view has hitherto been lacking. Here we show that female gametes of Aurelia aurita, the common jellyfish, do not transcribe mitochondrial DNA, lack electron transport, and produce no free radicals. In contrast, male gametes actively transcribe mitochondrial genes for respiratory chain components and produce ROS. Electron microscopy shows that this functional division of labour between sperm and egg is accompanied by contrasting mitochondrial morphology. We suggest that mitochondrial anisogamy underlies division of any animal species into two sexes with complementary roles in sexual reproduction. We predict that quiescent oocyte mitochondria contain DNA as an unexpressed template that avoids mutational accumulation by being transmitted through the female germ line. The active descendants of oocyte mitochondria perform oxidative phosphorylation in somatic cells and in male gametes of each new generation, and the mutations that they accumulated are not inherited. We propose that the avoidance of ROS-dependent mutation is the evolutionary pressure underlying maternal mitochondrial inheritance and the developmental origin of the female germ line.

The Fuel Cell Model of Abiogenesis: A New Approach to Origin-of-Life Simulations

“…The iron-nickel-sulfide-containing centers of the enzymes act as anodes and cathodes (Berg and Holm, 1982;Baymann et al 2003;Vignais and Billoud 2007); meanwhile, the membranes -capable as they are of selective ion transport -maintain chemical disequilibrium (Lane and Martin 2012). Derived from proteobacteria, the mitochondria bear certain similarities to chemiosmotic LUCA (Yang et al, 1985;Martin and Müller, 1998;de Paula et al 2013). LUCA's biological battery would have had some similar functional parts, such as the Complex I (referred to as the 'steam engine of the cell' by Efremov and Sazanov (2011)) that, through redox disequilibria, drives protons to the periplasm.…”

Implications of Non-Differentiable Entropy on a Space-Time Manifold

“…There are studies sustaining the avoidance of ROS-dependent mutation as an evolutionary pressure underlying maternal mitochondrial inheritance and the developmental origin of the female germ line [28]. Most interestingly, it has been postulated that the maintenance of any gene within a bioenergetic organelle may be the result of natural selection with a selective advantage for the individual organelle in its ability to respond to changes in the redox state of its bioenergetic membrane and to regulate the synthesis of proteins in the electron transport chain by means of gene expression [28]. Therefore, in complex systems, complex bioinformatic systems are required to ensure long-term species conservation.…”

Potential long-term risks associated with maternal aging (the role of the mitochondria)

“…Primordial oocytes are in a near-inactive state until adolescence; however, low levels of metabolism may occur, although data from the jellyfish Aurelia aurita suggest that no mitochondrial activity is present in the eggs themselves (21). Even if primordial oocytes have no metabolism as proposed, the mechanism of progressive damage of mtDNA still applies to the cumulus cells, suggesting that damage to these helper cells could lead to inefficient oogenesis in the egg (21). Either of these two mechanisms would probably lead to mistakes during meiosis and the increase in the number of eggs with chaotic mosaicism.…”

“…Lamarck proposed that organisms acquired traits from the environment and passed these to their offspring (i.e., that there was no protection of the germ-line) (21). Weismann contested this hypothesis and proposed that inheritance was protected from the environment by the production of ''gametes'' (21).…”