Protonic Capacitor: Elucidating the biological significance of mitochondrial cristae formation

Abstract

Lee for decades, it was not entirely clear why mitochondria develop cristae? the work employing the transmembrane-electrostatic proton localization theory reported here has now provided a clear answer to this fundamental question. Surprisingly, the transmembrane-electrostatically localized proton concentration at a curved mitochondrial crista tip can be significantly higher than that at the relatively flat membrane plane regions where the proton-pumping respiratory supercomplexes are situated. The biological significance for mitochondrial cristae has now, for the first time, been elucidated at a protonic bioenergetics level: 1) The formation of cristae creates more mitochondrial inner membrane surface area and thus more protonic capacitance for transmembrane-electrostatically localized proton energy storage; and 2) The geometric effect of a mitochondrial crista enhances the transmembraneelectrostatically localized proton density to the crista tip where the Atp synthase can readily utilize the localized proton density to drive ATP synthesis.

Mitochondrial energetics with transmembrane electrostatically localized protons: do we have a thermotrophic feature?

“…It was subsequently uncovered that the alkalophilic bacteria can effectively utilize the protonic thermal kinetic energy through "TELP at the liquid-membrane interface" in driving the synthesis of ATP molecules [8][9][10][11][13][14][15]53 .Biomembrane including the mitochondrial membrane typically carries "negatively-charged surface groups" at its two sides attracting ions including cations and/or protons and thus forming "electrical double layers" 54 as expected by the Gouy-Chapman theory 55 . As pointed out previously 5,7,13,22 , the membrane surface charges are "fixed" and their attracted ions including the associated electrical double layers are irrelevant to the membrane potential �ψ ; Consequently, the membrane-fixed surface-charges-attracted ions (including the electrical double layers) "do not contribute to the pmf " 56 in living organisms. The membrane-fixed surface charge-associated "electrical double layers" are there all the time even before the biomembrane is physiologically energized and even when the cells including mitochondria are completely dead.Our recent theoretical studies 5,7,22 and experimental work 3,19,49,57 showed a protonic capacitor: the formation of TELP demonstrated in an anode water-membrane-water cathode biomimetic system 19 .…”

“…As pointed out previously 5,7,13,22 , the membrane surface charges are "fixed" and their attracted ions including the associated electrical double layers are irrelevant to the membrane potential �ψ ; Consequently, the membrane-fixed surface-charges-attracted ions (including the electrical double layers) "do not contribute to the pmf " 56 in living organisms. The membrane-fixed surface charge-associated "electrical double layers" are there all the time even before the biomembrane is physiologically energized and even when the cells including mitochondria are completely dead.Our recent theoretical studies 5,7,22 and experimental work 3,19,49,57 showed a protonic capacitor: the formation of TELP demonstrated in an anode water-membrane-water cathode biomimetic system 19 . The experimental demonstration of the protonic capacitor provided a proof-of-principle for the creation of TELP, mimicking an energized biomembrane system such as a mitochondrion in its energized resting state 3 .…”

“…In this well-documented case, the application of the Mitchellian textbook pmf equation (Eq. 1) would predict a pmf of only 44 mV that for decades could never really explain how the organisms can synthesize ATP with such a "small pmf " 2,5,[33][34][35] .As previously reported 5,7,13,[20][21][22] , another deficiency of Mitchell's chemiosmotic theory is its failure in addressing the legitimate question on whether the protonic coupling pathway for oxidative phosphorylation is localized at the membrane surface or delocalized throughout the bulk aqueous phase since 1961 when this question was first raised by Williams [36][37][38][39][40][41][42][43] . We now know, Mitchell's delocalized proton view cannot explain a number of welldocumented experimental results including (but not limited to): (1) The "localized proton coupling characteristics" demonstrated in the "low salt" treated thylakoids of the well-documented Chiang-Dilley experiment 44 ; (2) The observed mitochondrial "ΔpH surface component of pmf " 45 ; (3) The "newly reported lateral pH gradient" along the mitochondrial inner membrane surface 46 ; (4) An independent biomimetic study 47 recently also showing a phenomenon of localized protons; and (5) The deficiency of Mitchell's chemiosmotic theory that could not fully explain the energetics even in mitochondria and E. coli as recently noticed by Lee and other scientists 5,13,20,48 .Furthermore, the novel transmembrane electrostatic proton localization (also called as TELP) theory 1,2,4-7,9,13 developed recently with biomimetic experimental demonstrations 3,19,49,50 showed how a "protonic capacitor" can form from excess protons at one side of a membrane with excess hydroxyl anions at the other side of the membrane.…”

Isothermal Environmental Heat Energy Utilization by Transmembrane Electrostatically Localized Protons at the Liquid–Membrane Interface

“…7 Through an application of the Lee transmembrane electrostatic proton localization theory, the bioenergetic significance of mitochondrial cristae formation has now also been successfully elucidated. 44 …”

The aerobic mitochondrial ATP synthesis from a comprehensive point of view

“…to considerably increase the surface of the inner membrane, increasing the efficiency of the OxPhos process. The cristae formation is functional to better functioning of membrane H + capacitor for better functionality of ATP synthase [ 29 ]. The H + handling was also analysed and it was found that bacterial phospholipid esters enable better H + lateral currents when in a monolayer over water than the isoprenoid phospholipid ethers of archaea [ 30 ].…”