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W2072236701 abstract "In Archaea, bacteria, and eukarya, ATP provides metabolic energy for energy-dependent processes. It is synthesized by enzymes known as A-type or F-type ATP synthase, which are the smallest rotatory engines in nature (Yoshida, M., Muneyuki, E., and Hisabori, T. (2001) Nat. Rev. Mol. Cell. Biol. 2, 669–677; Imamura, H., Nakano, M., Noji, H., Muneyuki, E., Ohkuma, S., Yoshida, M., and Yokoyama, K. (2003) Proc. Natl. Acad. Sci. U. S. A. 100, 2312–2315). Here, we report the first projected structure of an intact A1A0 ATP synthase from Methanococcus jannaschii as determined by electron microscopy and single particle analysis at a resolution of 1.8 nm. The enzyme with an overall length of 25.9 nm is organized in an A1 headpiece (9.4 × 11.5 nm) and a membrane domain, A0 (6.4 × 10.6 nm), which are linked by a central stalk with a length of ∼8 nm. A part of the central stalk is surrounded by a horizontal-situated rodlike structure (“collar”), which interacts with a peripheral stalk extending from the A0 domain up to the top of the A1 portion, and a second structure connecting the collar structure with A1. Superposition of the three-dimensional reconstruction and the solution structure of the A1 complex from Methanosarcina mazei Gö1 have allowed the projections to be interpreted as the A1 headpiece, a central and the peripheral stalk, and the integral A0 domain. Finally, the structural organization of the A1A0 complex is discussed in terms of the structural relationship to the related motors, F1F0 ATP synthase and V1V0 ATPases. In Archaea, bacteria, and eukarya, ATP provides metabolic energy for energy-dependent processes. It is synthesized by enzymes known as A-type or F-type ATP synthase, which are the smallest rotatory engines in nature (Yoshida, M., Muneyuki, E., and Hisabori, T. (2001) Nat. Rev. Mol. Cell. Biol. 2, 669–677; Imamura, H., Nakano, M., Noji, H., Muneyuki, E., Ohkuma, S., Yoshida, M., and Yokoyama, K. (2003) Proc. Natl. Acad. Sci. U. S. A. 100, 2312–2315). Here, we report the first projected structure of an intact A1A0 ATP synthase from Methanococcus jannaschii as determined by electron microscopy and single particle analysis at a resolution of 1.8 nm. The enzyme with an overall length of 25.9 nm is organized in an A1 headpiece (9.4 × 11.5 nm) and a membrane domain, A0 (6.4 × 10.6 nm), which are linked by a central stalk with a length of ∼8 nm. A part of the central stalk is surrounded by a horizontal-situated rodlike structure (“collar”), which interacts with a peripheral stalk extending from the A0 domain up to the top of the A1 portion, and a second structure connecting the collar structure with A1. Superposition of the three-dimensional reconstruction and the solution structure of the A1 complex from Methanosarcina mazei Gö1 have allowed the projections to be interpreted as the A1 headpiece, a central and the peripheral stalk, and the integral A0 domain. Finally, the structural organization of the A1A0 complex is discussed in terms of the structural relationship to the related motors, F1F0 ATP synthase and V1V0 ATPases. ATP synthases/ATPases are present in every life form and are the most important enzymes for the energy metabolism of the cell (1Yoshida M. Muneyuki E. Hisabori T. Nat. Rev. Mol. Cell. Biol. 2001; 2: 669-677Crossref PubMed Scopus (723) Google Scholar). They catalyze the formation of ATP at the expense of the transmembrane electrochemical ion gradient. They arose from a common ancestor that underwent structural and functional changes leading to three distinct classes of A1A0 1The abbreviations used are: A1A0 ATPase, Archaea-type ATPase; F1F0, F1F0 ATP synthase; V1V0 ATPase, vacuolar-type ATPase., F1F0, and V1V0 ATP synthases/ATPases. The V-type ATPases, found in organelles of eukaryotes, lost their ability to synthesize ATP. Their function is to create steep ion gradients at the expense of ATP hydrolysis (2Nelson N. Biochim. Biophys. Acta. 1992; 1100: 109-124Crossref PubMed Scopus (157) Google Scholar). Archaea contain ATPases, the A1A0 ATP synthases, that are structurally similar to V1V0 ATPases but synthesize ATP like the F-type ATPases. The genomic sequences available today show that the overall subunit composition of the A1A0 ATP synthases is very similar to the V1V0 ATPases. For example, the A1A0 ATP synthases contain duplicated and even triplicated K subunits (proteolipids) (3Müller V. Ruppert C. Lemker T. J. Bioenerg. Biomebr. 1999; 31: 15-28Crossref PubMed Scopus (53) Google Scholar, 4Müller V. Grüber G. Cell Mol. Life Sci. 2003; 60: 474-494Crossref PubMed Scopus (149) Google Scholar). The A1A0 ATP synthase has at least nine subunits (A3B3CDEFHIKX), but the actual subunit stoichiometry, especially regarding the proteolipid subunits K in A ATPases, is different in various organisms (12, 6, 4, or as suggested by genomic data, only 1 (5Müller V. J. Bioenerg. Biomembr. 2004; 36: 115-125Crossref PubMed Scopus (41) Google Scholar)). The A1A0 ATP synthase is composed of a water-soluble A1 ATPase and an integral membrane subcomplex, A0. ATP is synthesized or hydrolyzed on the A1 headpiece consisting of an A3B3 domain, and the energy that is provided for or released during that process is transmitted to the membrane-bound A0 domain (4Müller V. Grüber G. Cell Mol. Life Sci. 2003; 60: 474-494Crossref PubMed Scopus (149) Google Scholar). The energy coupling between the two active domains occurs via the so-called stalk part, an assembly proposed to be composed of the subunits C, D, and F (6Coskun Ü. Grüber G. Koch M.H.J. Godovac-Zimmermann J. Lemker T. Müller V. J. Biol. Chem. 2002; 277: 17327-17333Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Insight in the molecular structure of the A-type ATP synthases comes from small-angle x-ray scattering data of the A1 ATPase from Methanosarcina mazei Gö1 whose A1 domain is made up of the five different subunits, A3B3CDF (8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar). The data have shown that the hydrated A1 ATPase is rather elongated with a headpiece of 10 × 9.4 nm in dimension and a stalk of ∼8.4 nm in length. A comparison of the central stalk of this A1 complex with bacterial F1 and eukaryotic V1 ATPase indicates different lengths of the stalk domain (8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar, 9Svergun D.I. Konrad S. Huss M. Koch M.H.J. Wieczorek H. Altendorf K. Volkov V.V. Grüber G. Biochemistry. 1998; 37: 17659-17663Crossref PubMed Scopus (56) Google Scholar). Image processing of electron micrographs of negatively stained A1 ATPase from M. mazei Gö1 (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar) has revealed that the headpiece consists of a pseudohexagonal arrangement of six masses surrounding a seventh mass. These barrel-shaped masses of ∼3.2 and 2.8 nm in diameter and 7.5 and 5.0 nm in length, which consist of the major subunits A and B, are arranged in an alternating manner (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). The hexagonal barrel of subunits A and B encloses a cavity of ∼2.3 nm in the middle in which part of the central stalk is asymmetrically located. The stalk protrudes from the bottom side of the headpiece forming an angle of ∼20° with the vertical axis of the molecule. At the upper end of the hexagonal barrel, extensions can be observed that are assumed to belong to the N termini of subunit A (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Further insights into the topology of the A1 ATPase were obtained by differential protease sensitivity (8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar) and cross-linking studies (6Coskun Ü. Grüber G. Koch M.H.J. Godovac-Zimmermann J. Lemker T. Müller V. J. Biol. Chem. 2002; 277: 17327-17333Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). These studies resulted in a model in which the subunits C, D (partly), and F form the central stalk domain (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). However, in contrast to the related F- and V-type ATP synthases/ATPases, little is known regarding the overall structure of the A1A0 molecule, which is largely due to the instability of the isolated complexes (10Wilms R. Freiberg C. Wegerle E. Meier I. Mayer F. Müller V. J. Biol. Chem. 1996; 271: 18843-18852Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar). Most recently, an isolation procedure of the A1A0 ATP synthase of the hyperthermophilic Archaea Methanococcus jannaschii resulted in a complete and functionally coupled enzyme (11Lingl A. Huber H. Stetter K.O. Mayer F. Kellermann J. Müller V. Extremophiles. 2003; 7: 249-257Crossref PubMed Scopus (36) Google Scholar). Besides the property of being an enzyme of a hyperthermophilic organism whose multienzyme complexes are believed to be more stable than those of mesophiles, the M. jannaschii A1A0 ATP synthase is of particular interest because it has a K subunit three times the size of that of most bacteria and Archaea. Furthermore, this subunit has lost one of the ion translocating residues (12Ruppert C. Kavermann H. Wimmers S. Schmid R. Kellermann J. Lottspeich F. Huber H. Stetter K.O. Müller V. J. Biol. Chem. 1999; 274: 25281-25284Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar). Here, we used electron microscopy to visualize directly the structure of the A1A0 ATP synthase from M. jannaschii. A comparison with the low resolution structure of the A1 ATPase from M. mazei Gö1, derived from small-angle x-ray scattering data and single particle electron microscopy, allowed the unambiguous identification of most of the densities in the stalk domain and the A0 part. The structure of the complete A1A0 ATP synthase also facilitates, for the first time, a comparison with structural models of the related F1F0 ATP synthase and V1V0 ATPase holoenzymes. Materials—All of the chemicals were of reagent grade and were obtained from Merck (Darmstadt, Germany), BIOMOL (Hamburg, Germany), Roth (Karlsruhe, Germany), or Sigma (Deisenhofen, Germany). Protein Preparation—The A1A0 ATP synthase of M. jannaschii was purified by sucrose density centrifugation and anion-exchange chromatography (DEAE-Sepharose) as described previously (11Lingl A. Huber H. Stetter K.O. Mayer F. Kellermann J. Müller V. Extremophiles. 2003; 7: 249-257Crossref PubMed Scopus (36) Google Scholar). ATPase-active fractions were pooled and concentrated on Centricon 100-kDa concentrators (Millipore). The concentrated sample was loaded on a Superose 6 column (10/30, Amersham Biosciences) and eluted with 50 mm Tris-HCl (pH 7.5), 5 mm MgCl, 10% glycerine, 150 mm NaCl, 0.1% Triton X-100, 0.1 mm phenylmethylsulfonyl fluoride, and Pefabloc SC (a final concentration of 1 mm, BIOMOL). The peak fractions, which were stained with silver, were collected and analyzed by SDS-PAGE (13Schägger H. Cramer W.A. v. Jagow G. Anal. Biochem. 1994; 217: 220-230Crossref PubMed Scopus (1043) Google Scholar, 14Damerval C. le Guillioux M. Blaisomeau J. de Vienne D. Electrophoresis. 1987; 8: 158-159Crossref Scopus (159) Google Scholar). Mg2+-dependent ATPase activity was determined as described earlier (15Heinonen J.K. Lahti R.J. Anal. Biochem. 1981; 113: 313-317Crossref PubMed Scopus (789) Google Scholar). Electron Microscopy and Image Analysis—Protein was prepared on freshly glow-discharged carbon-coated copper grids stained with 2% uranyl acetate. Images of the negatively stained A1A0 ATP synthase were collected on a Philips CM20FEG electron microscope operating at 200 kV and liquid N2-cooled specimen to reduce radiation damage. Images of 2,048 × 2,048 pixels (after a binning of 2) were recorded at ×67,200 magnification at a pixel size of 30 μm with a Gatan 4000 SP 4K slow-scan CCD camera with GRACE software for semi-automated specimen selection and data acquisition (16Oostergetel G.T. Keegstra W. Brisson A. Ultramicroscopy. 1998; 74: 47-59Crossref Scopus (78) Google Scholar). Single particle analysis was performed with the GRIP (Groningen image processing) software package on a PC cluster. 2W. Keegstra, unpublished data. A total of 17,238 single particle projections (128 × 128 pixel frame; pixel size of 0.34 nm) from 331 images were obtained by selecting all of the discernable particles. For each micrograph, the defocus value was determined and a simple contrast transfer function correction by phase reversal was done (17Frank J. Penczek P. Optik. 1995; 98: 125-129Google Scholar). After band-pass filtering, the images were subsequently subjected to multireference alignment, multivariate statistical analysis, and hierarchical ascendant classification. This dataset was divided into two subsets including either one or two peripheral stalks to obtain a more homogenous dataset for a refinement of these classes. The subsets were analyzed in parallel by reference-free alignment (18Dube P. Bacher G. Stark H. Mueller F. Zemlin F. van Heel M. Brimacombe R. J. Mol. Biol. 1998; 279: 403-421Crossref PubMed Scopus (62) Google Scholar). Each rotational and translational alignment was repeated four times, and classification was done by multivariate statistical analysis. Datasets were again divided and aligned as described above. The final classification of the homogenous datasets was performed by multivariate statistical analysis and hierarchical classification to extract the key structural features of the enzyme (19van Heel M. Frank J. Ultramicroscopy. 1981; 6: 187-194PubMed Google Scholar). The resolution of the class averages was measured according to van Heel (20van Heel M. Ultramicroscopy. 1984; 13: 165-184Crossref PubMed Scopus (210) Google Scholar). Subunit Composition and Electron Microscopy—A characteristic gel of the preparation of the A1A0 ATP synthase from M. jannaschii is presented in Fig. 1A showing the nine subunits, A–F, H, I, and K, with apparent molecular masses of 66, 51, 45, 25, 23, 11, 10, 77, and 21 kDa, respectively. A typical electron microscopy raw image of the enzyme yields monodisperse particles with almost no contamination by smaller particles that could represent dissociated complexes or fragments (Fig. 1B). A total of 17,238 such molecular images were subjected to image processing. Fig. 2 demonstrates different class sums of the A1A0 ATP synthase projections obtained after several steps of reference-free translational/rotational alignment, multivariate statistical analysis, and multireference alignment. All of the projections reveal a tripartite structure consisting of a headpiece, a membrane-embedded domain, and a connecting stalk region. The classes can be grouped in respect to the number of visible stalks: one group showing one peripheral stalk besides the central stalk (Fig. 2, frames A1–4; 12,555 particles) and a second group with two peripheral stalks on both the left and right side (Fig. 2, frames B1–4; 4,683 particles). To obtain more homogeneous classes, both data sets, including either two or three stalks, were analyzed separately as described under “Experimental Procedures.” Fig. 3 shows averages of each refined data set at a resolution of 1.8 nm (Fig. 3, A–C). In all of the averages, the A1A0 ATP synthase from M. jannaschii has a total length of 25.9 nm. The dimensions of the A1 headpiece, the central stalk domain, and the membrane portion, A0, are 9.4 × 11.5, 8.0 × 3.9, and 6.4 × 10.6 nm, respectively. The A1 headpiece has a rather spherical mass that is clearly separated from the stalk domain at its base (Fig. 3B). The stalk domain is formed by a central stalk and either one (Fig. 3A) or two peripheral stalks (Fig. 3B). This observation might be explained either by some of the complexes being disrupted or by these classes containing complexes in different orientation. The central stalk can be divided into an asymmetric upper part and a collar-like structure located above the A0 domain. In the collar, several distinct densities could be resolved. At both ends of this domain, two of such densities are connected to the peripheral stalks (Fig. 3B), which go all the way up to the A1 headpiece. One of these stalks appears to be in close contact with two areas of the A1 headpiece with one located at the outside and the second located on top of the A3B3 headpiece (Fig. 3, B and C). This peripheral stalk shows a clear connection to the A0 portion via the collar structure (Fig. 3, B and C). By comparison, the second peripheral stalk is attached to the top of the A1 headpiece (Fig. 3C) and extended slightly down from the collar domain (Fig. 3B). A corresponding weak density rises up from the A0 (Fig. 3B). Whereas the peripheral stalk(s) seems to be connected to the outside of the A0 domain, the central stalk is attached to the center of the membrane-embedded A0, which appears as a rather symmetric flattened sphere and slightly tilted in most of the projections, especially in Fig. 2, frame B3.Fig. 2A gallery of selected classes resulting from the last multivariate statistical analysis and classification of 17,238 particles of the A1A0 ATP synthase. Four classes (1–4) showing either one (A) or two (B) peripheral stalk(s) besides the central stalk are shown.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Fig. 3Total averages calculated from 410 (A), 497 (B), and 316 (C) images. C, a projection at around 40° compared with that in B. Bar represents 20 nm. Labels: black arrows, masses of the peripheral stalks connected with the A1 headpiece; white arrowhead, asymmetric upper part of the central stalk; black asterisk, mass connecting the A0 with the collar like domain; white arrows, mass extending from the collar and the A0 domain.View Large Image Figure ViewerDownload Hi-res image Download (PPT) Localization of the Subunits Inside the A1A0 ATP Synthase—A known three-dimensional reconstruction of the asymmetrical A1 complex from M. mazei Gö1 (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar) determined from tilt pairs of negatively stained molecules was superimposed on the projection of the A1A0 ATP synthase from M. jannaschii (Fig. 4, panel C) by rotating the A1 subcomplex in 5° steps through 360°. One of the projections of the A1 from M. mazei Gö1 is well accommodated within the A1 headpiece, composed of the A3B3D subassembly (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar) and the upper central stalk, which is only partially (35%) solved in the three-dimensional reconstruction of the A1 ATPase from M. mazei Gö1 (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). In this projection, one of the catalytic A subunits is on the right of the A1 domain, implying that the peripheral stalk on the right may be close to this major A subunit. Nevertheless, from the superposition of the A1 profile with the A1 part in the A1A0 ATP synthase images, it is clear that the cap at the top of the A1 headpiece (Figs. 3B and 4C) does not belong to the A3B3D subassembly. To further examine the composition of the central stalk, the projection of the A1A0 ATP synthase from M. jannaschii was compared with the solution structure of the A3B3CDF complex of the A1 ATPase from M. mazei Gö1 deduced from solution x-ray scattering data (8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar). The central stalk of the hydrated A3B3CDF complex, which consists of the subunits C, F, and a part of subunit D, is 8.4 nm in length (8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar) and fits well to the dimensions (8 nm) of the elongated central stalk of the negative-stained A1A0 ATP synthase, indicating that the central stalk is made up by the subunits C, D (partly), and F. The A1A0 ATP synthase has been described as a chimeric enzyme combining the structural and functional features of F1F0 ATP synthases and V1V0 ATPases (4Müller V. Grüber G. Cell Mol. Life Sci. 2003; 60: 474-494Crossref PubMed Scopus (149) Google Scholar). Single particle analysis resulted in the visualization of projections of the A1A0 ATP synthase from M. jannaschii consisting of an A1 headpiece and an A0 domain linked by a central stalk and two peripheral stalks. The A1 headpiece fits well with the projection of the recently determined three-dimensional reconstruction with the A1 complex from M. mazei Gö1 composed of the hexagonal A3B3 domain surrounding a cavity in which the central stalk subunit D is located (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar, 8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar). The subunit is displaced toward an A-B-A triplet (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar), allowing the rearrangements of the central D subunit as demonstrated for the A1 ATPase from M. mazei Gö1 (6Coskun Ü. Grüber G. Koch M.H.J. Godovac-Zimmermann J. Lemker T. Müller V. J. Biol. Chem. 2002; 277: 17327-17333Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar) and the related Thermus thermophilus A1/V1 ATPase (21Imamura H. Nakano M. Noji H. Muneyuki E. Ohkuma S. Yoshida M. Yokoyama K. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 2312-2315Crossref PubMed Scopus (170) Google Scholar). A key feature from the superposition of the A1 complex from M. mazei Gö1 and the A1A0 ATP synthase is the close fit at the top of the A1 headpiece showing the knoblike structures. These knobs, also found in the related V-type ATPase (22Boekema E.J. Ubbink-Kok T. Lolkema J.S. Brisson A. Konings W.N. Photosyn. Research. 1998; 57: 267-273Crossref Scopus (22) Google Scholar, 23Wilkens S. Vasilyeva E. Forgac M. J. Biol. Chem. 1999; 274: 31804-31810Abstract Full Text Full Text PDF PubMed Scopus (128) Google Scholar, 24Grüber G. Radermacher M. Ruiz T. Godovac-Zimmermann J. Canas B. Kleine-Kohlbrecher D. Huss M. Harvey W.R. Wieczorek H. Biochemistry. 2000; 39: 8609-8616Crossref PubMed Scopus (69) Google Scholar, 25Domgall I. Venzke D. Luttge U. Ratajczak R. Böttcher B. J. Biol. Chem. 2002; 277: 13115-13121Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar) but absent in the F-type ATP synthases (26Wilkens S. Capaldi R.A. Biochim. Biophys. Acta. 1998; 1365: 93-97Crossref PubMed Scopus (75) Google Scholar, 27Böttcher B. Bertsche I. Reuter R. Gräber P. J. Mol. Biol. 2000; 296: 449-457Crossref PubMed Scopus (52) Google Scholar, 28Karrasch S. Walker J.E. J. Mol. Biol. 1999; 290: 379-384Crossref PubMed Scopus (99) Google Scholar), are formed by the N-terminal non-homologous inserts (80–90 amino acids) of the three catalytic A subunits, which alternate with the nucleotide-binding B subunits (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar, 29Grüber G. Wieczorek H. Harvey W.R. Müller V. J. Exp. Biol. 2001; 204: 2597-2605Crossref PubMed Google Scholar). They point out that the cap at the very top of the A1A0 molecule (Fig. 4C) is not formed by a subunit belonging to the soluble A1 domain (see below). The comparison of the A1A0 ATP synthase with the recently determined envelope of the M. mazei Gö1A3B3CDF complex in solution (8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar) yields that there is no significant shrinkage of the A1A0 molecule through the negative staining procedure. The central stalk is rather elongated (∼8 nm) and in close contact with A0. As described recently, the central stalk of the M. mazei Gö1 A3B3CDF complex accommodates subunits C, F, and partly D (7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar, 8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar). The cross-linking data of this complex indicate that subunit F is in close neighborhood to one of the nucleotide-binding B subunits (Fig. 5) and that F, together with the central stalk subunits C and D, undergoes significant structural rearrangements depending on nucleotide binding (6Coskun Ü. Grüber G. Koch M.H.J. Godovac-Zimmermann J. Lemker T. Müller V. J. Biol. Chem. 2002; 277: 17327-17333Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 7Coskun Ü. Radermacher M. Müller V. Ruiz T. Grüber G. J. Biol. Chem. 2004; 279: 22759-22764Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Such nucleotide-dependent alterations of stalk subunits C, D, and F will facilitate the mechanistic linkage of ATP synthesis/hydrolysis in the A3B3 hexamer to ion pumping in the A0 part via the central CDF stalk domain. The length and the shape of the central stalk of the A1 part resemble those of the related V1 ATPase (8Grüber G. Svergun D.I. Coskun Ü. Lemker T. Koch M.H.J. Schägger H. Müller V. Biochemistry. 2000; 40: 1890-1896Crossref Scopus (42) Google Scholar, 9Svergun D.I. Konrad S. Huss M. Koch M.H.J. Wieczorek H. Altendorf K. Volkov V.V. Grüber G. Biochemistry. 1998; 37: 17659-17663Crossref PubMed Scopus (56) Google Scholar). In contrast, the central stalk of the complete bacterial F1 ATPase is substantially shorter (4.0–4.5 nm) (9Svergun D.I. Konrad S. Huss M. Koch M.H.J. Wieczorek H. Altendorf K. Volkov V.V. Grüber G. Biochemistry. 1998; 37: 17659-17663Crossref PubMed Scopus (56) Google Scholar, 30Grüber G. J. Bioenerg. Biomembr. 2000; 32: 341-346Crossref PubMed Scopus (16) Google Scholar). The question that now arises is, which subunits of the A1A0 ATP synthase contribute to the A0 domain, the peripheral stalks, and the additional mass on top of A1. The A1A0 ATP synthase as isolated has nine subunits (A–I, K). Five of them form the A1 part and are assembled in the stoichiometry A3B3CDF (see above). The I and K subunits form the membrane domain, A0 (11Lingl A. Huber H. Stetter K.O. Mayer F. Kellermann J. Müller V. Extremophiles. 2003; 7: 249-257Crossref PubMed Scopus (36) Google Scholar, 12Ruppert C. Kavermann H. Wimmers S. Schmid R. Kellermann J. Lottspeich F. Huber H. Stetter K.O. Müller V. J. Biol. Chem. 1999; 274: 25281-25284Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar). Subunit I (70 kDa) is very similar to subunit a of V1V0 ATPases with a hydrophilic N-terminal and a hydrophobic C-terminal domain. The C terminus of subunit I is predicted to have seven transmembrane helices and is assumed to be functionally similar to subunit a of the V1V0 ATPases and F1F0 ATP synthases (3Müller V. Ruppert C. Lemker T. J. Bioenerg. Biomebr. 1999; 31: 15-28Crossref PubMed Scopus (53) Google Scholar). The N-terminal domain is predicted to be highly α-helical and assumed to be the functional homolog of the soluble domain of peripheral stalk subunit b of F1F0 ATP synthases. Because only one of the peripheral stalks is clearly attached to the outside of the A0 domain, we conclude that the hydrophilic N terminus of subunit I emerges from the membrane-embedded A0 part and may go up along the side of A1 until the top of the A1 headpiece (Fig. 5). Whether the N-terminal domain might partly contribute to the cap on the top of the A1A0 molecule can only be speculated. In the presented average, the peripheral stalk (right) has a kinked structure in the lower part, giving this domain the flexibility to wrap around the A1 headpiece and ending up as the cap on the top (Fig. 3, B and C). Insertion and deletion of altered length in the so-called “tether” domain of the peripheral stalk subunit b of the Escherichia coli F1F0 ATP synthase, which is located above the membrane service, can be tolerated by the enzyme, indicating that this related connecting stalk has an inherent flexible structure (31Grabar T.B. Cain B.D. J. Biol. Chem. 2003; 37: 34751-34756Abstract Full Text Full Text PDF Scopus (27) Google Scholar). It has been suggested for the F1F0 ATP synthases that flexibility of the domain might allow reorientation of the stalk to act as a stator for rotation in one direction during ATP synthesis and in the opposite direction during ATP hydrolysis (31Grabar T.B. Cain B.D. J. Biol. Chem. 2003; 37: 34751-34756Abstract Full Text Full Text PDF Scopus (27) Google Scholar, 32Hardy A.W. Grabar T.B. Bhatt D. Cain B.D. J. Bioenerg. Biomembr. 2003; 35: 389-397Crossref PubMed Scopus (11) Google Scholar). Subunit K is a homolog of the F-type subunit c with two transmembrane helices. It consists of fused tandem repeats of sequences corresponding to the F-type subunit. M. jannaschii has a subunit K with six membrane-spanning helices (27 kDa) but with only two active carboxylates per monomer (12Ruppert C. Kavermann H. Wimmers S. Schmid R. Kellermann J. Lottspeich F. Huber H. Stetter K.O. Müller V. J. Biol. Chem. 1999; 274: 25281-25284Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar), which are involved in ion conduction along the membrane. As in the case of the F-type ATP synthases (33Stock D. Gibbons C. Arechaga I. Leslie A.G. Walker J.E. Curr. Opin. Struct. Biol. 2000; 10: 672-679Crossref PubMed Scopus (265) Google Scholar, 34Vonck J. von Nidda T.K. Meier T. Matthey U. Mills D.J. Kühlbrandt W. Dimroth P. J. Mol. Biol. 2002; 321: 307-316Crossref PubMed Scopus (105) Google Scholar) and V-type ATPases (35Wilkens S. Forgac M. J. Biol. Chem. 2001; 276: 44064-44068Abstract Full Text Full Text PDF PubMed Scopus (83) Google Scholar), the K subunits (or c in the F- and V-type ATPases) are thought to form a ring, which belongs to the rotary element inside the A1A0 ATP synthase. As shown in Fig. 4, the bottom of the central CDF-stalk domain spans the upper center of the A0 domain, facilitating the direct contact of the rotary elements, which consists of an ensemble made from the central stalk (CDF domain) and a ring of hydrophobic K subunits in the A0 membrane domain (21Imamura H. Nakano M. Noji H. Muneyuki E. Ohkuma S. Yoshida M. Yokoyama K. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 2312-2315Crossref PubMed Scopus (170) Google Scholar). The second peripheral stalk appears to be connected to the collar domain and goes up to the A1 headpiece. Probable candidates for this stalk are the remaining A1A0-hydrophilic subunits H (12 kDa) and E (25 kDa) with the latter predicted to be highly α-helical (12Ruppert C. Kavermann H. Wimmers S. Schmid R. Kellermann J. Lottspeich F. Huber H. Stetter K.O. Müller V. J. Biol. Chem. 1999; 274: 25281-25284Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar). The modest contact area of this peripheral stalk with the A1 headpiece, which is also evident in electron micrographs of the related bacterial V1V0 ATPase from Caloramator fervidus (36Boekema E.J. van Bremen J.F.L. Brisson A. Ubbink-Kok T. Konings W.N. Lolkema J.S. Nature. 1999; 401: 37-38Crossref PubMed Scopus (76) Google Scholar), might be caused partially by stain accumulation. The top view projection of the rotated A1 complex (Fig. 4, panel D) shows a groove at the top of the A3B3-hexamer in close neighborhood to this peripheral stalk. Such a groove-like feature may form a binding domain for the peripheral connection in the A1 headpiece. In general, the positions of the peripheral stalks of the A1A0 ATP synthase as deduced from side views cannot be directly verified from top view projections, because such projection are not present in significant numbers if intact A1A0 molecules are prepared. In summary, the first two dimensional projection maps of the A1A0 ATP synthase from M. jannaschii presented provides the structural basis toward a fuller understanding of the mechanistic events occurring in this class of enzymes. The reconstruction at a 1.8-nm resolution shows similarities and diversities between the structural modules to the evolutionary-linked F1F0 ATP synthases and V1V0 ATPases, such as the catalytic A1/F1/V1 headpiece and the central stalk domain. Although the existence of one (26Wilkens S. Capaldi R.A. Biochim. Biophys. Acta. 1998; 1365: 93-97Crossref PubMed Scopus (75) Google Scholar, 37Rubinstein J.L. Walker J.E. Henderson R. EMBO J. 2003; 22: 6182-6192Crossref PubMed Scopus (187) Google Scholar) or two (27Böttcher B. Bertsche I. Reuter R. Gräber P. J. Mol. Biol. 2000; 296: 449-457Crossref PubMed Scopus (52) Google Scholar) peripheral stalk(s) in the F1F0 ATP synthase is uncertain, these classes of ATPases/synthases might need at least one peripheral stalk acting as a stator that prevents the major hexameric arranged subunits (α3β3 or A3B3) from following the rotation of the central stalk domain. Whether the visualized second peripheral stalk in the V1V0 ATPase and in the presented A1A0 ATP synthase might act as a regulatory domain in the A-type ATP synthase as described for the plant V ATPase (25Domgall I. Venzke D. Luttge U. Ratajczak R. Böttcher B. J. Biol. Chem. 2002; 277: 13115-13121Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar) can now be addressed." @default.
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W2072236701 title "Structure and Subunit Arrangement of the A-type ATP Synthase Complex from the Archaeon Methanococcus jannaschii Visualized by Electron Microscopy" @default.
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