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Bioenergetics in Mitochondria, Bacteria and Chloroplasts

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Bioenergetics in Mitochondria, Bacteria and Chloroplasts Bioenergetics in Mitochondria, Bacteria and Chloroplasts Bioenergetics in Mitochondria, Bacteria and Chloroplasts Third Joint German/UK Bioenergetics Conference, a Biochemical Society Focused Meeting held at Schloss Rauischholzhaschholzhausen,usen, Ebsdorfergrund, Germany,Germany, 10–13 April 2013. Organized and Edited by Fraser MacMillan (University of East Anglia, Norwich, U.K.) and Thomas Meiereier ((MaxMax Planck Institute of Biophysics,BiophBiop ysic Frankfurt am Main, Germany). Half a century of molecular bioenergetics Wolfgang Junge*1 s.org *Niedersachsen-Professur f ¨ur Biophysik, Fachbereich Biologie/Chemie, Universititat ¨¨at Osnabrsnabrruck, ¨¨uck, 49069 Osnabrnabrruck,uc ¨¨uck, Germany Abstract Molecular bioenergetics deals with theconstruction, function and regulation oof the powerhouses of life. The present overview sketches sceneses and actors,ctors, farsightedffarsighted goals and ddaring hypotheses, meticulous tool-making, painstaking benchwork,enchwork, luckyucky discovery, serious scepticism, emphatic believing and strong characters with weak and othersthers with hardard arguments, told from a personal, admittedly limited, perspective. Bioenergetics will blossom further withh the search focused on o both where there is bright light for ever-finer detail and the obvious darkark spotspots for surprise and discovery.r Copy Introduction operative oxygen binding (for which he was awarded the Early research into ‘bioenergetics’, the energy supply for life, Nobel Prize in Chemistry in 1962). At this time, only a started in the 18th8th Century.ry. Jan Ingen-Housz [1] discovereddisco few proteins involved in photosynthesis and respiration were that plantsproduce biomass at the expense of sunsunlight, the known; none was structurally resolved or only crystallized. ultimateenergy source,urce, and water plus gases, ththe substrates. Those proteins were black boxes scattered over a wide open, In hisstudy on vegetables, Ingen-Housz noticed their “great but highly relevant, research field. It has attracted scientists powerwer of purifying the common air in the sunshine and from a broad range of disciplines. off injuringng it in the shade andan at nignight” [1]. It was a first Molecular bioenergetics started with the analysis of uthorspectroscopic Copy signatures and reaction rates. In 1955, elements appreciationeciationon of the productionproduc and re-consumption in the reactioncycle cle betweenbe photosyphotosynthesis and respiration of of the respiratory electron transport from various substrates what was later coined ‘oxygen’ and ‘carbon dioxide’. More to oxygen were tracked by Britton Chance and Ron Williams than twocenturies later, Karl Lohmann (in 1929) discovered [5,6] who monitored transients of pigment cofactors. AuthorPhotosynthesis CopyCo was more difficult to tackle owing to the ATP, VladimirEngelhart (in 1935) found that it powers muscle activity, and Fritz Lipmann (between 1939 and 1941) higher speed of its partial reactions. This complication emphasized “energy-rich phosphate bonds” as the main was then compensated by the benefit of non-invasive carriers of chemical energy in the cell. David Keilin [2] and stimulation by short light pulses. In 1961, three biophysicists, Otto Warburg [3] were the first to discover proteins involved Lou Duysens [7], Bessel Kok [8] and Horst Witt [9], in respiration, namely cytochrome c and ‘Atmungsferment’, independently concluded that green plant photosynthesis alias cytochrome c oxidase, respectively. is powered by two photosystems which, acting in a serial Max Perutz’s programmatic article entitled ‘Proteins, the electron transport chain, drive electrons from water to + machines of life’ [4] set the path for today’s molecular NADP . PSII (Photosystem II) oxidizes water to yield understanding of life. His work on the crystal structure oxygen and protons. It reduces PSI (Photosystem I) which, + of haemoglobin revealed, for the first time, structural in turn, reduces NADP to NADPH. The comprehension determinants of protein function, here the mechanics of co- between biophysicists, who studied spectroscopic transients, and biochemists, who were after the ‘real’ products, was Key words: cell respiration, electron transport, molecular bioenergetics, phosphorylation, almost nil. When confronted with Witt’s reaction scheme photosynthesis, proton transport. at a conference in 1962, Warburg mused: “Could you tell Abbreviations used: pmf, protonmotive force; PSI, Photosystem I; PSII, Photosystem II. 1 email [email protected] us how the chemical mechanism of photosynthesis can be °C °C Biochemical Biochemical Society Transactions www.biochemsoctran Biochem. Soc. Trans. (2013) 41, 1207–1218; doi:10.1042/BST20130199 The Authors Journal compilation 2013BiochemicalSociety 1207 1208 BiochemicalSocietyTransactions(2013)Volume41,part 5 described on the basis of your spectroscopic observations?” Figure 1 Light absorption, excitation energy transfer and Witt countered with a well-aimed jibe at his eminent critic, trapping the pioneer of oxygen detection, by observing that “it would High quantum yield despite large variations between antennae systems be difficult to deduce the mechanism of a combustion engine (see the text for details andreferences). Chlorosome structural model based only on sniffing the exhaust” (see [10]). The detailed by Alfred Holzwarth (http://www.cec.mpg.de/forschung/h.cec.mpg.deg.de eterogene- analysis of the respective electron transport chains progressed reaktionen/photochemistry.html)tml) [148,149];49]; LHLH2 (light-harvesting rapidly owing to new tools in spectroscopy (e.g. pulsed lasers, complex 2) model byRichard Cogdell (http://www.gla.ac.uk/ EPR) and rapid kinetics, as pioneered by Manfred Eigen, researchinstitutes/biology/staff/richardcogdell/researchinterests/ Ronald Norrish, George Porter (joint winners of the Nobel lh2complex/lh2imagegallaries/lh2imagegallerywholecomplex/) [150]. Prize in Chemistry in 1967) and Britton Chance (see his fascinating account in [11]). The atomic structure of the pertinent membrane proteins Starting from Max Perutz’s programme in 1945, it took moreorere than two decades until the photosynthetic reaction centre of a purple bacterium was solubilized in functional form [12], and it took another two decades until Johann Deisenhofer, Robert Huber and Hartmut Michel (joint winners off the Nobel Prize in Chemistry in 1988) published a first structuraltructural modelmode at 3 A˚ (1 A˚ = 0.1 nm) resolution [13]. It was thefirst structurestr of any membrane protein ever. A decade later, at a legendary Bioenergetics Gordon Conference in 1995, at which Hartmut Michel had already presentedresented his structuraltructural model of bacterial cytochrome c oxidase [14], Shinya Yoshikawa described his yet to be publisheded structure of a mammalian oxidaseo [15] (for its properties,erties,s, see the article by Peter Rich andan colleagues in thishis issue of Biochemical SocietySociet or TransactionsTransac Copy [15a]). Shortly beforeefore Yoshikawa’s talk ended, the unexpected coincidence of twowo new structures was rightly underscored by fireworkseworks for the Fourth of July celebrationscelebratio outside the thin-walled audience. Today, structural models are available {ENDOR (electron nuclear double resonance) [23]} and for all of thee proteins of respirationrespir and photosynthesis. The theoretical chemistry (density functional theory [24]), seem to largest is PSI from green plants with a molecular mass of converge towards one particular structural model of the metal 660 kDa, hosting almost 200 chlorophyll molecules [16]. The centre and its ligands, including water (-derivatives). X-ray similarly large ATP synthase is the most agile machine of crystal structural analysis may soon take up and challenge or all. By mechanic transmission, a rotary chemical generator corroborate this concept by a novel ‘probe before destroy’ [17] is mechanically coupled to a rotary electrochemical approach where a PSII crystal is exposed to the ultra-short motorotorr ([18,19]([1 and see below). Whether complex I, a and intense X-ray pulse (100 fs) of a free-electron laser [25]. super-stoichiometric-stoichiomestoi proton pump in mitochondria, operates Structural detail on the Mn Ca moiety with bound water by similarly pronouncedp mid-range mechanical interactions 4 derivatives is a requisite to disclose the detailed reaction [20] has still to be established (see the articles by Leo mechanism of this ‘holy grail’ of photosynthesis. Sazanov and Volker Zickermann in this issue of Biochemical Society Transactions [20a,20b]). PSII, the water–quinone oxidoreductase, has revealed its protein structure at 1.9 A˚ Common principles govern the transfer of resolution (see [21] and references therein). When clocked by excitation in photosynthesis and of flashes of light, its catalytic Mn4Ca cluster steps through four electrons in photosynthesis and respiration sequentially higher oxidation states until (in 1 ms) the reaction Molecular bioenergetics has blossomed into an unforeseen with bound water proceeds to yield dioxygen. The pooling of resolution of its machinery not only in space (2 A˚ ), but also four oxidizing equivalents before initiating the four-electron in time (<1 ps). The painstaking elucidation of complexity reaction with water controls hazardous intermediates (e.g. has been a prerequisite to fully appreciate the remarkable hydroxyl radical and superoxide) on the way to dioxygen. The simplicity and robustness of Nature’s engineering. Two Mn4Ca cluster proper has
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