YidC Is Involved in the Biogenesis of Anaerobic Respiratory Complexes in the Inner Membrane of Escherichia coli

YidC of Escherichia coli belongs to the evolutionarily conserved Oxa1/Alb3/YidC family. Members of this family have all been implicated in membrane protein biogenesis of aerobic respiratory and energy-transducing proteins. YidC is essential for the insertion of subunit c of the F1F0-ATP synthase and subunit a of cytochrome o oxidase. The aim of this study was to investigate whether YidC plays a role during anaerobic growth of Escherichia coli, specifically when either nitrate or fumarate are used as terminal electron acceptors or under fermentative conditions. The effect of YidC depletion on the growth, enzyme activities, and protein levels in the inner membrane was determined. YidC is essential for all anaerobic growth conditions tested, and this is not because of the decreased levels of F1F0-ATP synthase in the inner membrane only. The results suggest a role for YidC in the membrane biogenesis of integral membrane parts of the anaerobic respiratory chain. YidC of Escherichia coli belongs to the evolutionarily conserved Oxa1/Alb3/YidC family. Members of this family have all been implicated in membrane protein biogenesis of aerobic respiratory and energy-transducing proteins. YidC is essential for the insertion of subunit c of the F1F0-ATP synthase and subunit a of cytochrome o oxidase. The aim of this study was to investigate whether YidC plays a role during anaerobic growth of Escherichia coli, specifically when either nitrate or fumarate are used as terminal electron acceptors or under fermentative conditions. The effect of YidC depletion on the growth, enzyme activities, and protein levels in the inner membrane was determined. YidC is essential for all anaerobic growth conditions tested, and this is not because of the decreased levels of F1F0-ATP synthase in the inner membrane only. The results suggest a role for YidC in the membrane biogenesis of integral membrane parts of the anaerobic respiratory chain. In Escherichia coli about 30% of all encoded proteins are located in the inner and outer membranes. The cytoplasmic or inner membrane contains essential energy-transducing complexes such as components of the electron transport chain, as well as solute transporters. Most integral inner membrane proteins are inserted co-translationally via the general secretory pathway otherwise known as the Sec system. In this pathway ribosome-bound nascent chains are targeted by the bacterial signal recognition particle to the SecYEG translocase via the signal recognition particle receptor FtsY. The membrane insertion of these proteins proceeds by a co-translational “threading mechanism” (1.de Gier J.W. Luirink J. Mol. Microbiol. 2001; 40: 314-322Crossref PubMed Scopus (82) Google Scholar) in which the accessory protein YidC might play an important role in the clearance of transmembrane segments (TMSs) 2The abbreviations used are: TMS, transmembrane segment; PMF, proton motive force; IMV, inner membrane vesicle. from the SecYEG channel (2.Samuelson J.C. Chen M. Jiang F. Moller I. Wiedmann M. Kuhn A. Phillips G.J. Dalbey R.E. Nature. 2000; 406: 637-641Crossref PubMed Scopus (428) Google Scholar). A small subset of integral membrane proteins are targeted directly to YidC where they are integrated into the membrane in a Sec-independent manner. YidC belongs to the evolutionarily conserved Oxa1/Alb3/YidC family. Oxa1 (oxidase assembly) from yeast was the first member of this family to be described. It was originally identified as an essential factor for the biogenesis of respiratory complexes in the mitochondrion (3.Bauer M. Behrens M. Esser K. Michaelis G. Pratje E. Mol. Gen. Genet. 1994; 245: 272-278Crossref PubMed Scopus (109) Google Scholar, 4.Bonnefoy N. Chalvet F. Hamel P. Slonimski P.P. Dujardin G. J. Mol. Biol. 1994; 239: 201-212Crossref PubMed Scopus (182) Google Scholar), more specifically the insertion of subunits of the cytochrome bc1 oxidase and ATP synthase. Alb3 is located in the thylakoid membranes of Arabidopsis chloroplasts (5.Moore M. Harrison M.S. Peterson E.C. Henry R. J. Biol. Chem. 2000; 275: 1529-1532Abstract Full Text Full Text PDF PubMed Scopus (189) Google Scholar) and is involved in the biogenesis of light-harvesting complexes. Members of the family have all been implicated in membrane protein biogenesis of respiratory and energy-transducing proteins. In E. coli it has been shown that YidC is essential for the insertion of subunit c of the F1F0-ATP synthase (Foc) (6.van der Laan M. Bechtluft P. Kol S. Nouwen N. Driessen A.J. J. Cell Biol. 2004; 165: 213-222Crossref PubMed Scopus (178) Google Scholar) and subunit a of cytochrome o oxidase (CyoA) (7.du Plessis D.J. Nouwen N. Driessen A.J. J. Biol. Chem. 2006; 281: 12248-12252Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 8.van Bloois E. Haan G.J. de Gier J.W. Oudega B. Luirink J. J. Biol. Chem. 2006; 281: 10002-10009Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar). Although the effect of YidC depletion on the insertion of respiratory proteins has been studied in aerobically grown E. coli cells, the same has not been done for anaerobically grown cells. In the absence of oxygen, E. coli is able to use other organic (fermentation) and inorganic (anaerobic respiration) molecules as terminal electron acceptors. Nitrate is commonly used as an alternative electron acceptor to oxygen, and the protein complex nitrate reductase (NarGHI) replaces the cytochrome o oxidase. The α and β subunits, NarG and NarH, respectively, are located in the cytoplasm and attach to the membrane via the γ subunit NarI to form the nitrate reductase complex (9.Bertero M.G. Rothery R.A. Palak M. Hou C. Lim D. Blasco F. Weiner J.H. Strynadka N.C. Nat. Struct. Biol. 2003; 10: 681-687Crossref PubMed Scopus (412) Google Scholar). E. coli can also use fumarate as a terminal electron acceptor. The structure of fumarate reductase (FrdABCD) is similar to that of nitrate reductase except that the integral membrane part consists of two smaller subunits, namely FrdC and -D (10.Cecchini G. Schroder I. Gunsalus R.P. Maklashina E. Biochim. Biophys. Acta. 2002; 1553: 140-157Crossref PubMed Scopus (206) Google Scholar). Although another translocation pathway, the Tat system (Twin Arginine Translocation), has been shown to target the peripheral αβ subcomplex to the integral membrane γ subunit of some anaerobic respiratory complexes, for example the DMSO reductase (DmsABC) (11.Sambasivarao D. Dawson H.A. Zhang G. Shaw G. Hu J. Weiner J.H. J. Biol. Chem. 2001; 276: 20167-20174Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar), this is not the case for all terminal reductases such as the fumarate reductase (11.Sambasivarao D. Dawson H.A. Zhang G. Shaw G. Hu J. Weiner J.H. J. Biol. Chem. 2001; 276: 20167-20174Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar). Also, how the integral membrane γ subunits of these complexes are inserted into the membrane is not known. In E. coli only three natural substrates of YidC have been identified, namely Foc, CyoA, and more recently the ion channel MscL (12.Facey S.J. Neugebauer S.A. Krauss S. Kuhn A. J. Mol. Biol. 2007; 365: 995-1004Crossref PubMed Scopus (93) Google Scholar). The identification of additional inner membrane proteins, which rely solely on YidC for their insertion, would give insight into the insertion mechanism of YidC and a possible evolutionarily conserved function of the Oxa1/Alb3/YidC family. The aim of this study was to investigate whether YidC plays a role in the membrane biogenesis of anaerobic respiratory complexes, i.e. the complexes essential for growth when either nitrate or fumarate is used as a terminal electron acceptor or under fermentative conditions. Our data demonstrate that YidC is essential for all growth conditions tested and that this is not only because of decreased levels of F1F0-ATP synthase in the inner membrane. The results suggest a role for YidC in the membrane biogenesis of integral membrane subunits of the anaerobic respiratory chain. Bacterial Strains and Plasmids—The YidC depletion strain E. coli FTL10 (MC4100-A, ΔyidC, attB::(araC+, PBAD, yidC+) KanR) (13.Hatzixanthis K. Palmer T. Sargent F. Mol. Microbiol. 2003; 49: 1377-1390Crossref PubMed Scopus (103) Google Scholar) was a generous gift of Frank Sargent (University of East Anglia, Norwich, UK). Strains E. coli SF100 (F–lacX74 galE galK thi rpsL (strA) ΔphoA(pvuII), ΔompT) and NN100 (SF100, lpp D(uncB-C) zid::Tn10) (14.Nouwen N. van der Laan M. Driessen A.J. FEBS Lett. 2001; 508: 103-106Crossref PubMed Scopus (31) Google Scholar) were used to test dependence of anaerobically grown cells on the F1F0-ATPase. Plasmid pTrc99A (15.Amann E. Brosius J. Gene (Amst.). 1985; 40: 183-190Crossref PubMed Scopus (308) Google Scholar) was used to construct plasmid pET589 containing E. coli yidC (16.Nouwen N. Driessen A.J. Mol. Microbiol. 2002; 44: 1397-1405Crossref PubMed Scopus (137) Google Scholar). E. coli FTL10 was transformed with plasmids pTrc99A and pET589 to construct “YidC–” and “YidC+” depletion strains when grown on glucose-containing media. Materials—Potassium nitrate was purchased from Fluka, and zinc powder, lapachol, and sodium fumarate were from Sigma. Texas Red was purchased from Invitrogen. Antiserum against YidC was raised in chickens against purified His-tagged YidC (Agrisera AB, Sweden). Antisera against fumarate reductase subunits FrdA and FrdB, the nitrate reductase complex (NarGHI), subunit c of the F1F0-ATP synthase (Foc), leader peptidase (LepB), phage shock protein A (PspA), and subunit K of the NADH dehydrogenase I (NuoK) were generous gifts from Joel Weiner (University of Alberta, Canada), Axel Magalon (LCB-IBSM CNRS, Marseille, France), Gabriele Deckers-Hebestreit (University of Osnabruckç Germany), Jan Tommassen (Utrecht University, The Netherlands), William Wickner (Dartmouth Medical School, Hanover, NH), and Takao Yagi (The Scripps The was purchased from and the nitrate test from was purchased from and were purchased from Sigma. Bacterial and were grown anaerobically on anaerobic growth with yeast as J. PubMed Google Scholar). The electron and were as sodium sodium and sodium and sodium were only when nitrate was used an electron acceptor. cells of E. coli FTL10 either plasmid pET589 or pTrc99A was grown aerobically in anaerobic growth containing were in anaerobic growth and in anaerobic growth containing or and nitrate or sodium fumarate as and growth was to an of to The cells were with the same and the was the of the strain from J. D. G. J. PubMed Scopus Google Scholar). membrane were from these cells as A. Driessen A.J. van der C. PubMed Scopus Google Scholar). was these The and nitrate of the growth were growth in the in E. coli strains SF100 and NN100 were first grown aerobically in anaerobic growth containing The cells were in anaerobic growth and into the same containing the of electron and used under conditions. The was of growth under anaerobic conditions. and were with the protein as a and were to Nature. PubMed Scopus Google Scholar, T. J. S. A. PubMed Scopus Google Scholar). for were with of inner membrane and were were in in of was as PubMed Scopus Google Scholar). Nitrate reductase and fumarate reductase of were a The were by the of in the of nitrate or fumarate R.A. I. G. Weiner J.H. J. PubMed Scopus Google Scholar). The were in an anaerobic with a under The of was to be and was as of nitrate or fumarate of of a Sec translocase was with Texas as a der Laan M. Nouwen N. Luirink J. Driessen A.J. 2001; PubMed Scopus Google Scholar). K was the translocation to of YidC to the of under YidC is for protein biogenesis of respiratory and proteins under anaerobic the growth of E. coli FTL10 (13.Hatzixanthis K. Palmer T. Sargent F. Mol. Microbiol. 2003; 49: 1377-1390Crossref PubMed Scopus (103) Google Scholar) under anaerobic conditions in the of electron acceptors and either pET589 or pTrc99A were grown as under the of the strain from J. D. G. J. PubMed Scopus Google Scholar). The of electron acceptors and were nitrate and nitrate and fumarate and fumarate and the strain to under all conditions tested of growth was cells an of the cells been of cells by and for and that the cells were the and nitrate in the growth not used and which the growth of the strain growth cells were grown anaerobically in the of the and electron acceptor to an of and with and the was the of the strain as under cells were grown anaerobically in the of the and electron acceptor to an of and with and the was the of the strain as under in a YidC of the inner membrane protein that YidC depletion The levels of the inner membrane protein leader peptidase (LepB), which is not on YidC for insertion, are by YidC depletion as by The levels of YidC were by against The of the on the against YidC were and the were and with against which was used as a membrane The of the of YidC were as the of the YidC and the to levels of YidC in the membrane was for all in the that the levels of YidC in from strains grown in the same growth for a of in the Sec by YidC in E. coli are in the that that YidC depletion not the translocation of proteins via the Sec or the Tat pathway (13.Hatzixanthis K. Palmer T. Sargent F. Mol. Microbiol. 2003; 49: 1377-1390Crossref PubMed Scopus (103) Google Scholar, Jiang F. Chen M. B. A. Dalbey R.E. 2003; PubMed Scopus Google Scholar, der Laan M. Nouwen N. Oudega B. N. Driessen A.J. Luirink J. S. A. 2003; PubMed Scopus Google Scholar). from anaerobically cells, the translocation of Texas in The of is which can be to a of the proton motive because a similar effect is when the and are of Texas from the was when ATP is data for anaerobically grown cells that the depletion not the levels of the Sec of YidC with the of c of the is a well studied of The levels of in were to YidC depletion under all anaerobic growth conditions tested The of were tested to that the F1F0-ATP synthase was not It has been shown that of the of can be to the F1F0-ATP synthase. van de the of from cells under all growth conditions is with to the The in YidC depletion was cells grown in with nitrate or fumarate and where was the YidC of in with aerobically grown E. coli cells, YidC depletion to a of the shock can be by against the that YidC depletion under anaerobic growth the was when with that under aerobic growth conditions YidC of the of F1F0-ATP in the test whether the of growth under conditions under anaerobic conditions can be to the in the levels of F1F0-ATP synthase in the E. coli NN100 and SF100 strains were grown in the same growth under conditions. E. coli strain NN100 is a of strain SF100 and contains a of the in a strain with F1F0-ATP synthase (14.Nouwen N. van der Laan M. Driessen A.J. FEBS Lett. 2001; 508: 103-106Crossref PubMed Scopus (31) Google Scholar). were grown anaerobically and the was of growth the growth of NN100 cells in containing only was cells able to anaerobically in all other growth The of the F1F0-ATP synthase is essential only under fermentative conditions and not for anaerobic growth with the electron acceptors with nitrate as the electron acceptor of NN100 a SF100 cells grown under the same that a of the in the of a F1F0-ATP synthase that the and of Nitrate in YidC the decreased levels of F1F0-ATP synthase in the membrane are not for the of growth the depletion of YidC the of some other for anaerobic when nitrate or fumarate are the electron other essential the protein levels and enzyme of other complexes essential for growth when nitrate or fumarate are the electron namely the nitrate and fumarate reductases and the NADH dehydrogenase I. In the absence of oxygen, E. coli can use alternative electron acceptors to form an electron transport chain. In the of and levels of the of the nitrate reductase containing is P. J. PubMed Scopus Google Scholar). an against the that the levels of YidC depletion The of the nitrate reductase was also by the of a lapachol, under anaerobic conditions. conditions the of nitrate by is The of nitrate reductase was in from cells in with cells. cells, nitrate reductase was in the and for cells the was of the nitrate and fumarate reductases as by of in the of electron acceptors nitrate or of membrane are as of nitrate or fumarate of are the of three with are as of nitrate or fumarate of are the of three with in a and of in YidC the same as for the nitrate reductase the effect of YidC depletion on another terminal fumarate was of was against the α and β subunits of the reductase and The data that the levels of FrdA and YidC Also, fumarate reductase of as by the of was to YidC depletion with nitrate the of fumarate reductase was in from cells in with cells. cells, fumarate reductase was in the and for cells, the was of the NADH I of the in cells results in a and protein of the F1F0-ATP synthase and complex the D. M. J. J. Mol. Biol. 2007; PubMed Scopus Google Scholar). E. coli two of NADH NADH dehydrogenase I consists of subunits located the inner encoded by the of the subunits are integral membrane proteins with the of from to The protein NADH dehydrogenase encoded by the is and YidC depletion under aerobic conditions has effect on der Laan M. Nouwen N. Oudega B. N. Driessen A.J. Luirink J. S. A. 2003; PubMed Scopus Google Scholar). anaerobic conditions in the of can in J. D. G. J. PubMed Scopus Google Scholar), and NADH dehydrogenase be used as a for the YidC depletion effect on these complexes. NADH dehydrogenase I is under all anaerobic conditions is important only during growth in the of fumarate J. D. G. J. PubMed Scopus Google Scholar). NADH dehydrogenase I more to complex I NADH dehydrogenase of small subunit K a subunit with three is a possible YidC of was against The data that the levels of YidC The data in this study demonstrate that under E. coli is to anaerobically with either nitrate or fumarate as electron acceptors. The levels of essential protein complexes were to possible for the of Although some in the membrane protein were the under conditions the that membrane proteins of It has been shown that the Sec translocase the Tat complex is by YidC depletion in E. coli FTL10 (13.Hatzixanthis K. Palmer T. Sargent F. Mol. Microbiol. 2003; 49: 1377-1390Crossref PubMed Scopus (103) Google Scholar, der Laan M. Nouwen N. Oudega B. N. Driessen A.J. Luirink J. S. A. 2003; PubMed Scopus Google Scholar). that is on YidC Jiang F. Chen M. B. A. Dalbey R.E. 2003; PubMed Scopus Google Scholar), the translocation of secretory proteins is only by YidC depletion in aerobically grown cells (2.Samuelson J.C. Chen M. Jiang F. Moller I. Wiedmann M. Kuhn A. Phillips G.J. Dalbey R.E. Nature. 2000; 406: 637-641Crossref PubMed Scopus (428) Google Scholar). test conditions of anaerobic growth, the Sec translocase also and the levels of a Sec are by YidC was only which can be to a of membranes to a In anaerobically cells, the can be to the decreased levels of membrane and of the F1F0-ATP synthase that is solely for the of a under conditions Deckers-Hebestreit G. K. J. Biol. Chem. Full Text PDF PubMed Google Scholar). YidC is essential for the insertion of and CyoA, YidC depletion under aerobic growth conditions results in a of der Laan M. Nouwen N. Oudega B. N. Driessen A.J. Luirink J. S. A. 2003; PubMed Scopus Google Scholar). is in to conditions that in the of the A.J. Mol. Microbiol. PubMed Scopus Google Scholar). in this has been on aerobically grown E. coli cells, study has shown that under the protein is not when cells are grown anaerobically A. S.A. K. J. 2006; PubMed Scopus Google Scholar). Our data are in with this study as the of under the anaerobic growth conditions tested is when with aerobically grown cells. are as to the mechanism by which the proteins in the the to with the of the study in E. coli that and the to anaerobic and the and of the G. A.J. M. J. Biol. Chem. 2006; 281: Full Text Full Text PDF PubMed Scopus Google Scholar). other on and E. coli only an of the in the and not a to anaerobic to the of the J. E. A.J. Mol. Microbiol. 2007; PubMed Scopus (32) Google Scholar, G. P. A. J.C. M. J. Biol. Chem. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). The mechanism by which proteins is under aerobic as well as anaerobic growth conditions. anaerobic conditions and in the of electron from to nitrate is to the of a (9.Bertero M.G. Rothery R.A. Palak M. Hou C. Lim D. Blasco F. Weiner J.H. Strynadka N.C. Nat. Struct. Biol. 2003; 10: 681-687Crossref PubMed Scopus (412) Google Scholar, J. PubMed Scopus Google Scholar). fumarate the fumarate reductase is directly for proton translocation (10.Cecchini G. Schroder I. Gunsalus R.P. Maklashina E. Biochim. Biophys. Acta. 2002; 1553: 140-157Crossref PubMed Scopus (206) Google Scholar). A of the levels of fumarate and nitrate reductases and of the F1F0-ATP synthase in the YidC depletion strain in a of the and of ATP these anaerobically grown cells can ATP by the of or a B. M. Escherichia coli and and for Scholar, B. M. Escherichia coli and and for Scholar), the F1F0-ATP synthase is not essential for ATP under these anaerobically conditions. the strain E. coli NN100 was able to with either nitrate or fumarate as an electron acceptor. It was shown that the protein levels and of the nitrate and the fumarate reductases were YidC be for the growth The α and β subunits of the nitrate NarG and NarH, respectively, are located and attach to the integral membrane γ subunit NarI to form the nitrate reductase complex (9.Bertero M.G. Rothery R.A. Palak M. Hou C. Lim D. Blasco F. Weiner J.H. Strynadka N.C. Nat. Struct. Biol. 2003; 10: 681-687Crossref PubMed Scopus (412) Google Scholar). or have Tat or signal T. J.C. M. Mol. Microbiol. 2002; PubMed Scopus Google Scholar) S. G. Nat. 2007; PubMed Scopus Google NarG a that to be a of the Tat Sargent F. J. Microbiol. 2004; PubMed Scopus Google Scholar). It has been that which is in the same as is a that the NarG and complex to the NarI Biophys. 2006; PubMed Scopus Google Scholar). In the same study it was that the growth of cells in was in the E. coli with a study that that anaerobic growth with nitrate was not in a E. coli strain (11.Sambasivarao D. Dawson H.A. Zhang G. Shaw G. Hu J. Weiner J.H. J. Biol. Chem. 2001; 276: 20167-20174Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar). whether of the dehydrogenase would have effect on growth in The Tat pathway has been implicated in the membrane of anaerobic respiratory complexes, which have an structure where the αβ subunits are located (11.Sambasivarao D. Dawson H.A. Zhang G. Shaw G. Hu J. Weiner J.H. J. Biol. Chem. 2001; 276: 20167-20174Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar, F. Palmer T. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar), for the The β subunit of this enzyme has TMS, which is inserted by the Tat translocase and which is (13.Hatzixanthis K. Palmer T. Sargent F. Mol. Microbiol. 2003; 49: 1377-1390Crossref PubMed Scopus (103) Google Scholar, A. Sargent F. FEBS Lett. 2003; PubMed Scopus Google Scholar). The αβ subunits attach and in the absence of the integral membrane γ subunit because of this located of the β subunit A. Sargent F. FEBS Lett. 2003; PubMed Scopus Google Scholar). In the nitrate reductase NarG has a and they NarI to attach to the membrane. reductase also has an structure with FrdA and a located αβ subcomplex that to the membrane via the integral membrane proteins FrdC and The in the levels of FrdA and with the inner membrane is of a role for YidC in the insertion of FrdC and because FrdA and the bacterial membrane first the of integral membrane parts FrdC and D.J. Weiner J.H. Cell Biol. PubMed Scopus Google Scholar). FrdC and are small and three proteins that have their located in the cytoplasm and their in the C. G. PubMed Scopus Google Scholar). some other anaerobic respiratory fumarate reductase has been shown to be of the Tat system for membrane and (11.Sambasivarao D. Dawson H.A. Zhang G. Shaw G. Hu J. Weiner J.H. J. Biol. Chem. 2001; 276: 20167-20174Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar). It has recently been that from cells not to be for the insertion of complex the structure is to fumarate reductase D. M. J. J. Mol. Biol. 2007; PubMed Scopus Google Scholar). The levels of of the NADH dehydrogenase I were also YidC were shown to in the levels were decreased because of YidC dependence for insertion, it would have a NADH dehydrogenase as of the peripheral of the complex is also the subunit is E. A. Yagi T. 44: PubMed Scopus Google Scholar). to or be for the of growth under conditions in the of a study an YidC and Bloois E. de de Gier J.W. Luirink J. FEBS Lett. PubMed Scopus Google Scholar), to the that NADH dehydrogenase I be Although it has been shown in this study and by that the Sec translocase the Tat complex is by YidC depletion in E. coli other of YidC depletion that the membrane and insertion of the in this The other identified YidC only is essential only under conditions. a in the membrane and of other membrane proteins, as for the transport involved in the of nitrate and to the growth in cells from YidC S. J. Cell Biol. 2004; 165: PubMed Scopus Google Scholar). on the insertion and of the integral membrane components of the nitrate and fumarate reductase complexes as well as of the NADH dehydrogenase I. Joel Weiner (University of Alberta, Canada), Axel Magalon (LCB-IBSM CNRS, Marseille, France), Gabriele Deckers-Hebestreit (University of Osnabruckç Germany), Jan Tommassen (Utrecht University, The Netherlands), William Wickner (Dartmouth Medical School, Hanover, NH), and Takao Yagi (The Scripps for the also de and for Plessis for the Texas and van der for of the with

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