The c13 Ring from a Thermoalkaliphilic ATP Synthase Reveals an Extended Diameter Due to a Special Structural Region

Matthies, Doreen; Preiß, Laura; Klyszejko, Adriana L.; Müller, Daniel J.; Cook, Gregory M.; Vonck, Janet; Meier, Thomas

doi:10.1016/j.jmb.2009.03.052

Cited by 71 publications

(60 citation statements)

References 41 publications

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“…This work not only suggested that a and b were not interdigitated with c but also revealed the surprising stoichiometry of c 10 . The Cterminal helix of the hairpin c subunit is at the outside of the ring and contains an essential aspartate or glutamate residue.…”

Section: P/o and Atp Synthase Structurementioning

confidence: 75%

“…On the other hand, this trio of alanines is not observed in lower eukarya and eubacteria (1), or in thylakoids, which have bigger rings. For the case of c 13 in an alkalophilic bacillus species, a different variant stretch of sequence contributes to an enlarged ring diameter (10). A further interesting aspect described in ref.…”

Section: P/o and Atp Synthase Structurementioning

confidence: 90%

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ATP synthase: From sequence to ring size to the P/O ratio

Ferguson

2010

Proc. Natl. Acad. Sci. U.S.A.

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Section: P/o and Atp Synthase Structurementioning

confidence: 75%

Section: P/o and Atp Synthase Structurementioning

confidence: 90%

ATP synthase: From sequence to ring size to the P/O ratio

Ferguson

2010

Proc. Natl. Acad. Sci. U.S.A.

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“…A few c-rings in these images were seen to lack individual c-subunits; however, instead of closing this gap so as to form smaller c-rings, these incomplete oligomers have the same shape and diameter as the complete ones (10,25). Furthermore, c-subunits from I. tartaricus and Bacillus TA2.A1 expressed in E. coli were found to assemble correctly into c 11 and c 13 rings, respectively (20,23,24,48), despite the preferred c 10 stoichiometry of the native E. coli c-ring (46). The c-ring sizes also are independent of external factors such as medium pH, host protein expression (48) or host membrane composition (23,24), the source of carbon used by the cell (48,49), and, importantly, the rate of ATP synthesis itself (50,51).…”

Section: Discussionmentioning

confidence: 90%

“…The majority of c/c-subunit interface contacts (see Table S2) are hydrophobic interactions, complemented by several hydrogen (H)-bonds and ion pairs in the vicinity of the Na + /H + -binding site and in the solvent-exposed areas of the molecule. Nevertheless, the high-resolution structure of the Bacillus pseudofirmus OF4 c 13 ring (18), with an AxAxAxA motif (19), and the projection map for the Caldalkalibacillus thermarum TA2.A1 (Bacillus TA2.A1) c 13 ring (20), with AxGxSxGxS, demonstrate that variations of the GxGxGxGxG motif can influence the structure of the c-rings and were developed, for example, as alkaliphilespecific adaptations of the Bacillus genus. Point mutations of dimerization domains have been shown to influence the association free energy of transmembrane α-helices (21).…”

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confidence: 99%

Engineering rotor ring stoichiometries in the ATP synthase

Pogoryelov¹,

Klyszejko

Krasnoselska³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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ATP synthase membrane rotors consist of a ring of c-subunits whose stoichiometry is constant for a given species but variable across different ones. We investigated the importance of c/c-subunit contacts by site-directed mutagenesis of a conserved stretch of glycines (GxGxGxGxG) in a bacterial c 11 ring. Structural and biochemical studies show a direct, specific influence on the c-subunit stoichiometry, revealing c <11 , c 12 , c 13 , c 14 , and c >14 rings. Molecular dynamics simulations rationalize this effect in terms of the energetics and geometry of the c-subunit interfaces. Quantitative data from a spectroscopic interaction study demonstrate that the complex assembly is independent of the c-ring size. Real-time ATP synthesis experiments in proteoliposomes show the mutant enzyme, harboring the larger c 12 instead of c 11 , is functional at lower ion motive force. The high degree of compliance in the architecture of the ATP synthase rotor offers a rationale for the natural diversity of c-ring stoichiometries, which likely reflect adaptations to specific bioenergetic demands. These results provide the basis for bioengineering ATP synthases with customized ion-to-ATP ratios, by sequence modifications.alpha helix packing | F 1 F o ATP synthase | membrane protein | rotary motor stoichiometry | bioenergetics

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“…However, alkaliphilic bacteria have also developed several adaptation strategies, which in combination support robust growth at high pH (12,13,17,18). These adaptations include alkaliphile-specific features of the ATP synthase, including changes at the c-ring's ion-binding site (19) as well as its size and stoichiometry (19)(20)(21). The N-terminal α-helix of the c-subunits contains a typical membrane protein-packing motif (22) of repetitive glycine residues (GxGxGxG) (Fig.…”

mentioning

confidence: 99%

The c-ring stoichiometry of ATP synthase is adapted to cell physiological requirements of alkaliphilic Bacillus pseudofirmus OF4

Preiß

Klyszejko

Hicks

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The c-rings of ATP synthases consist of individual c-subunits, all of which harbor a conserved motif of repetitive glycine residues (GxGxGxG) important for tight transmembrane α-helix packing. The cring stoichiometry determines the number of ions transferred during enzyme operation and has a direct impact on the ion-to-ATP ratio, a cornerstone parameter of cell bioenergetics. In the extreme alkaliphile Bacillus pseudofirmus OF4, the glycine motif is replaced by AxAxAxA. We performed a structural study on two mutants with alanine-to-glycine changes using atomic force microscopy and X-ray crystallography, and found that mutants form smaller c 12 rings compared with the WT c 13 . The molar growth yields of B. pseudofirmus OF4 cells on malate further revealed that the c 12 mutants have a considerably reduced capacity to grow on limiting malate at high pH. Our results demonstrate that the mutant ATP synthases with either c 12 or c 13 can support ATP synthesis, and also underscore the critical importance of an alanine motif with c 13 ring stoichiometry for optimal growth at pH >10. The data indicate a direct connection between the precisely adapted ATP synthase c-ring stoichiometry and its ionto-ATP ratio on cell physiology, and also demonstrate the bioenergetic challenges and evolutionary adaptation strategies of extremophiles.

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The c13 Ring from a Thermoalkaliphilic ATP Synthase Reveals an Extended Diameter Due to a Special Structural Region

Cited by 71 publications

References 41 publications

ATP synthase: From sequence to ring size to the P/O ratio

ATP synthase: From sequence to ring size to the P/O ratio

Engineering rotor ring stoichiometries in the ATP synthase

The c-ring stoichiometry of ATP synthase is adapted to cell physiological requirements of alkaliphilic Bacillus pseudofirmus OF4

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