The Origin of Membrane Bioenergetics

Abstract

Harnessing energy as ion gradients across membranes is as universal as the genetic code. We leverage new insights into anaerobe metabolism to propose geochemical origins that account for the ubiquity of chemiosmotic coupling, and Na(+)/H(+) transporters in particular. Natural proton gradients acting across thin FeS walls within alkaline hydrothermal vents could drive carbon assimilation, leading to the emergence of protocells within vent pores. Protocell membranes that were initially leaky would eventually become less permeable, forcing cells dependent on natural H(+) gradients to pump Na(+) ions. Our hypothesis accounts for the Na(+)/H(+) promiscuity of bioenergetic proteins, as well as the deep divergence between bacteria and archaea.

Wavy membranes and the growth rate of a planar chemical garden: Enhanced diffusion and bioenergetics

“…The evolution of ion-tight biological membranes was contingent on the prior invention of active ion pumping, or chemiosmosis (7,35,36). Long before the emergence of chemiosmosis with its active mechanism of ion transport, waviness constitutes a natural passive mechanism for the enhancement of transport across a semipermeable membrane that in our view forms part of the answer to the puzzle of the origin of membrane bioenergetics (33) and thereby the passage from passive osmosis in a hydrothermal vent vesicle to active chemiosmosis in a protocell. There is a vast distance between a chemical garden membrane and LUCA, but the fact that LUCA still needed a leaky membrane even at that much later stage in that climb in complexity (7) demonstrates what a vital aspect this ion transport mechanism constituted for protolife.…”

“…Indeed, there is an apparent paradox at the heart of the earliest protobiochemistry. A membrane had both to protect the complex chemistry from its environment yet at the same time to allow the passage of materials; to be at once permeable to some ions and so allow mixing, but at the same time to maintain steep pH gradients (7,33,34). Waviness provides a plausible mechanism to achieve enhanced transport across relatively thick abiotic hydrothermal vent membranes at the very beginnings of the climb in complexity toward life.…”

Early Microbial Evolution: The Age of Anaerobes

“…The core bioenergetic reaction of methanogens (reduction of CO 2 to methane) occurs spontaneously at alkaline hydrothermal vents today (Lang et al 2010;Etiope et al 2011;McCollom and Seewald 2013;Schrenk et al 2013). The chemiosmosis dependence of their carbon and energy metabolism when growing on H 2 and CO 2 is readily understood in terms of the geochemical origin of chemiosmotic gradients at alkaline hydrothermal vents (Lane and Martin 2012). Their carbon and energy metabolism is replete with transition metal catalysis (Sousa and Martin 2014).…”

“…Alkaline hydrothermal vents, like Lost City, generate natural pH gradients at the interface between their hydrothermal effluent and ocean water. Once proteins had arisen in evolution, such naturally generated ion gradients could have been harnessed for energy conservation, even before ion pumping mechanisms had been invented (Martin and Russell 2007;Lane and Martin 2012;Sojo et al 2014), which would go a long way to explaining why the rotor-stator type adenosine triphosphate (ATP)ase is as universal among genomes as the ribosome is; it was present in the universal common ancestor. The closer we look at carbon and energy in hydrothermal vents, the greater the similarities between geochemistry and the biochemistry of acetogens and methanogens (anaerobic autotrophs) become (Sousa and Martin 2014).…”

Senomic view of the cell: SenomeversusGenome

“…All life known on this planet is cellular. It is the assembly of lipid membranes that allowed the emergence of cellular life [90–92]. Membrane-based senes give all organisms their agency which is the central feature for their acting as genuinely living organisms.…”