ATP synthase: Evolution, energetics, and membrane interactions

Abstract

The synthesis of ATP, life’s “universal energy currency,” is the most prevalent chemical reaction in biological systems and is responsible for fueling nearly all cellular processes, from nerve impulse propagation to DNA synthesis. ATP synthases, the family of enzymes that carry out this endless task, are nearly as ubiquitous as the energy-laden molecule they are responsible for making. The F-type ATP synthase (F-ATPase) is found in every domain of life and has facilitated the survival of organisms in a wide range of habitats, ranging from the deep-sea thermal vents to the human intestine. Accordingly, there has been a large amount of work dedicated toward understanding the structural and functional details of ATP synthases in a wide range of species. Less attention, however, has been paid toward integrating these advances in ATP synthase molecular biology within the context of its evolutionary history. In this review, we present an overview of several structural and functional features of the F-type ATPases that vary across taxa and are purported to be adaptive or otherwise evolutionarily significant: ion channel selectivity, rotor ring size and stoichiometry, ATPase dimeric structure and localization in the mitochondrial inner membrane, and interactions with membrane lipids. We emphasize the importance of studying these features within the context of the enzyme’s particular lipid environment. Just as the interactions between an organism and its physical environment shape its evolutionary trajectory, ATPases are impacted by the membranes within which they reside. We argue that a comprehensive understanding of the structure, function, and evolution of membrane proteins—including ATP synthase—requires such an integrative approach.

Ferroportin 3 is a dual‐targeted mitochondrial/chloroplast iron exporter necessary for iron homeostasis in Arabidopsis

“…As metal transporters of the same family generally retain the direction of transport in respect to the cytoplasm, an organellar FPN is likely to transport iron into the organellar lumen. According to the endosymbiotic origin of mitochondria and chloroplasts (Roger et al, 2017; Yoon et al, 2004; Zimorski et al, 2014), it is possible that proteins of these organelles could retain their ancestral directionality, as seen in respiratory proteins (Nirody et al, 2020). Under the hypothesis that FPN3 is of bacterial origin, its directionality is consistent with iron export from its ancestral cytoplasm, that is, from the organellar lumen into the eukaryotic cytoplasm.…”

Mitochondrial compartmentalization: emerging themes in structure and function

“…The F 1 F O -ATP synthase comprises a membrane-bound H + -driven rotary motor (the F O sector) and a matrix-localized catalytic domain (the F 1 sector) connected by central and peripheral stalks (Figure 1D) [22,23]. In addition to producing the majority of ATP in eukaryotic cells, mitochondrial F 1 F O -ATP synthases also shape crista morphology by assembling as arrays of dimers along the crest of lamellar cristae and along lengths of tubular cristae [24][25][26][27].…”

Insights into lipid-protein interactions from computer simulations

“…A prominent example is the clustering of mitochondrial ATP synthase dimers along the highly curved crista ridges and their depletion in the flat stretches of the inner membrane (Blum et al 2019;Kuhlbrandt 2015). Still, many aspects of ATP synthase function in relation to curvature remain elusive, such as how the dimers remain anchored at specific membrane regions, and whether the curved environment influences its catalytic activity (Nirody et al 2020). Estimates of membrane curvature free energy are well within the range required for protein conformational changes, suggesting that the elastic energy stored in the membrane may be able to allosterically regulate a vast assortment of membrane proteins (Brown 2012;Golani et al 2019;Iversen et al 2015).…”