Abstract
A fundamental first step in the evolution of eukaryotes was infolding of the chemiosmotic membrane of the endosymbiont. This allowed the proto-eukaryote to amplify ATP generation while constraining the volume dedicated to energy production. In mitochondria, folding of the inner membrane has evolved into a highly regulated process that creates specialized compartments (cristae) tuned to optimize function. Internalizing the inner membrane also presents complications in terms of generating the folds and maintaining mitochondrial integrity in response to stresses. This review describes mechanisms that have evolved to regulate inner membrane topology and either preserve or (when appropriate) rupture the outer membrane.
Highlights
There is compelling evidence that energy is the primary driver of evolution (Lane, 2015)
Crista contents, including cytochrome c, spill into the cyosol, resulting in irreversible loss of membrane potential and ATP production (Mootha et al, 2001). Matrix swelling in this case was attributed (Feldmann et al, 2000) to the mitochondrial permeability transition pore, MPTP, the opening of which can drive an osmotic influx of water sufficient to unfold the inner membrane and rupture the outer membrane (e.g., Rasola and Bernardi, 2011)
Swelling of the matrix caused by osmotic influx of water compresses the cristae before significant pressure is applied to the outer membrane by outward expansion of the inner membrane
Summary
There is compelling evidence that energy is the primary driver of evolution (Lane, 2015). Because there are practical limits to the volume fraction that cells can reserve for mitochondria, crista packing is maximized where energy demand is greatest, e.g., in cardiomyocytes the surface area of the inner membrane is more than tenfold that of the outer membrane. Conditions that swell the matrix will cause the inner membrane to unfold and, eventually, rupture the outer membrane.
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