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

Abstract

This study employing the latest theory on transmembrane electrostatic proton localization has now, for the first time, consistently elucidated a decades-longstanding bioenergetic conundrum in alkalophilic bacteria and more importantly discovered an entirely new feature: isothermal environmental heat utilization by electrostatically localized protons at the liquid–membrane interface. It was surprisingly revealed that the protonic motive force (equivalent to Gibbs free energy) from the isothermal environmental heat energy utilization through the electrostatically localized protons is not constrained by the overall energetics of the redox-driven proton pump system because of the following: (a) the transmembrane electrostatically localized protons are not free to move away from the membrane surface as a protonic capacitor feature; (b) the proton pumps embedded in the cell membrane extend beyond the localized proton layer apparently as an asymmetric property of the biological membrane; and (c) the protonic inlet mouth of the ATP synthase that accepts protons is located within this layer as another natural property of the asymmetric biological membrane. This work has now, for the first time, shown a novel thermotrophic feature where biological systems can isothermally utilize environmental heat energy through transmembrane electrostatically localized protons to help drive ATP synthesis.

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

“…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.…”

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x www.nature.com/scientificreports/ pseuodofirmus) [27][28][29] that keep "their internal pH about 2.3 units more acidic than the ambient bulk pH while ∆ψ is about 180 mV" 2,5,13,[30][31][32] . In this well-documented case, the application of the Mitchellian textbook pmf equation (Eq.

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“…Surprisingly, large pmf values were found which substantially exceed the chemical energy upper limit of the redox-driven protonic pumps 10,11,14,15 . 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.…”

“…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 by Bal et al 58 , such a few (< 7) protons in the intermembrane/cristae space bulk liquid phase are obviously not sufficient to support the activities of ATP synthesis in a mitochondrion where "thousands of ATP synthase complexes are considered to be simultaneously active" 59 . We now understand, it is the large numbers of TELP (in a range from 1.84 × 10 4 to 7.36 × 10 4 protons) per mitochondrion that we have just recently calculated apparently play an essential role in helping driving ATP synthesis 7 .More importantly as mentioned above, through the energetics analysis using the TELP theory 1,2,4-7,9,13 , we recently discovered that "the alkalophilic bacteria are not only chemotrophs, but also have a thermotrophic feature that can create significant amounts of Gibbs free energy through isothermal utilization of environmental heat energy with TELP (protonic thermal motion kinetic energy) to do useful work such as driving ATP synthesis" 13 .What we recently discovered in the protonic energetics of alkalophilic bacteria 13 is just a tip of the iceberg. We now understand that the thermotrophic feature may occur in many protonic bioenergetic systems including mitochondria, which produce the cellular fuel ATP to support complex life 60 .…”