Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 Å resolution

Belrhali, Hassan; Nollert, Peter; Royant, Antoine; Menzel, Christoph; Rosenbusch, Jürg P.; Landau, Ehud M.; Pebay‐Peyroula, Eva

doi:10.1016/s0969-2126(99)80118-x

Cited by 445 publications

(419 citation statements)

References 36 publications

(65 reference statements)

Supporting

Mentioning

398

Contrasting

Unclassified

Order By: Relevance

“…The crystal structures of M indicating only one [23] or two water molecules [11,24] in the D85/D212 region, as compared to three water molecules in the bR resting state [1,2], suggest that in M the active-site water molecules may have an enhanced mobility, or may relocate to other sites. To assess the role of water molecules on the energetics of proton transfer from D85 back to the retinal Schiff base we performed QM/MM calculations of proton transfer paths with various numbers of active-site water molecules, and QM computations on gas-phase models of the D85/water interactions.…”

Section: Role Of Internal Water Moleculesmentioning

confidence: 97%

See 1 more Smart Citation

Mechanism of a proton pump analyzed with computer simulations

2009

View full text Add to dashboard Cite

Understanding the mechanism of proton pumping requires a detailed description of the energetics and sequence of events associated with the proton transfers, and of how proton transfer couples to conformational rearrangements of the protein. Here, we discuss our recent advances in using computer simulations to understand how bacteriorhodopsin pumps protons. We emphasize the importance of accurately describing the retinal geometry and the location of water molecules.

show abstract

Section: Role Of Internal Water Moleculesmentioning

confidence: 97%

“…The retinal chromophore is covalently bound via a protonated Schiff base to K216. In the low-temperature crystal structures of the bR resting state [1,2] the Schiff base hydrogen bonds to water molecule w402, which in turn hydrogen bonds to the negatively charged D85 and D212 (Fig. 1).…”

Section: Introductionmentioning

confidence: 99%

Mechanism of a proton pump analyzed with computer simulations

2009

View full text Add to dashboard Cite

show abstract

“…In addition to the bacterial RC, a few proteins have now been crystallized that have been found to possess bound lipids (27). Bacteriorhodopsin was found to contain several lipids, although this protein was crystallized by using lipids unlike most other proteins (28). A few lipids have been reported for cytochrome c oxidase (29,30), FhuA (31), and photosystem I (32).…”

Section: Model Of Quasiproteins In Membranesmentioning

confidence: 99%

Interactions between lipids and bacterial reaction centers determined by protein crystallography

Cámara-Artigas

Brune

Allen

2002

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

140

118

View full text Add to dashboard Cite

The structure of the reaction center from Rhodobacter sphaeroides has been solved by using x-ray diffraction at a 2.55-Å resolution limit. Three lipid molecules that lie on the surface of the protein are resolved in the electron density maps. In addition to a cardiolipin that has previously been reported [McAuley, K. E., Fyfe, P. K., Ridge, J. P., Isaacs, N. W., Cogdell, R. J. & Jones, M. R. (1999) Proc. Natl. Acad. Sci. USA 96, 14706 -14711], two other major lipids of the cell membrane are found, a phosphatidylcholine and a glucosylgalactosyl diacylglycerol. The presence of these three lipids has been confirmed by laser mass spectroscopy. The lipids are located in the hydrophobic region of the protein surface and interact predominately with hydrophobic amino acids, in particular aromatic residues. Although the cardiolipin is over 15 Å from the cofactors, the other two lipids are in close contact with the cofactors and may contribute to the difference in energetics for the two branches of cofactors that is primarily responsible for the asymmetry of electron transfer. The glycolipid is 3.5 Å from the active bacteriochlorophyll monomer and shields this cofactor from the solvent in contrast to a much greater exposed surface evident for the inactive bacteriochlorophyll monomer. The phosphate atom of phosphatidylcholine is 6.5 Å from the inactive bacteriopheophytin, and the associated electrostatic interactions may contribute to electron transfer rates involving this cofactor. Overall, the lipids span a distance of Ϸ30 Å, which is consistent with a bilayer-like arrangement suggesting the presence of an ''inner shell'' of lipids around membrane proteins that is critical for membrane function.I ntegral membrane proteins are found in the cell membrane surrounded by lipids. The biophysical and biochemical properties of these proteins are critically determined by the lipid environment. The lipid composition of cell membranes is complex, containing a variety of phospholipids, glycolipids, and other small molecules. In the purple nonsulfur bacterium Rhodobacter sphaeroides, the major lipids are the phospholipids, phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, and cardiolipin, or diphosphatidyl glycerol, and two glycolipids, sulfoquinovosyl diacylglycerol and glucosylgalactosyl diacylglycerol (1). The relative amounts of these lipids vary significantly depending on specific growth conditions, in particular the oxygen level, although the fatty acid chains are always predominately 18:1 with only minor contributions from 18:0, 16:0, and 16:1 and trace amounts of smaller chains. The lipid composition is known to critically determine the morphology of the cell membrane, but whether the lipids can affect the photosynthetic energy conversion processes remains an outstanding question.Understanding the influence of the lipid properties on the photosynthetic complexes, or any other integral membrane proteins, is in most cases limited by the lack of detailed structural information concerning membrane proteins. To ...

show abstract

“…A fourth water may be present according to ref. 41, which will be denoted by W409*. These two mostprobable possibilities are investigated separately, which yield H ϩ ⅐(H 2 O) 3 and H ϩ ⅐(H 2 O) 4 WLANs together with the excess proton.…”

mentioning

confidence: 99%

Structures and spectral signatures of protonated water networks in bacteriorhodopsin

Mathias

Marx

2007

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

137

144

View full text Add to dashboard Cite

Networks of internal water molecules are thought to provide proton transfer pathways in many enzymatic and photosynthetic reactions. Extremely broad absorption continua observed in recent IR spectroscopic measurements on the photodriven proton pump bacteriorhodopsin (BR) suggest such networks may also serve as proton storage and release sites for these reactions. By combining electronic structure calculations with molecular mechanical force fields, we examine the dynamics and the resulting IR spectra of two protonated water networks, H ؉ ⅐(H2O)3 and H ؉ ⅐(H2O)4, in the release pocket of the initial state of BR, which possibly serve as proton donors to the extracellular surface. For both network sizes, topologically similar structures are found, which are anchored at residues E194 and E204 and stabilized by additional hydrogen bonds from neighboring protein side chains. These protonated water networks assume neither the classic Zundel nor Eigen motives but prefer wire-like topologies. Upon gauging calculated IR spectra of finite clusters with experimental gas-phase data, it is possible to link spectral features computed for these chain-like structures in the initial state of the BR photocycle to the measured absorption continua, in particular for the larger H ؉ ⅐(H2O)4 network. Furthermore, the free energy of proton dislocation along these chains is found to be within the range that is easily accessible at room temperature because of fluctuations.hydrogen-bonded networks ͉ hybrid molecular dynamics ͉ proton transport ͉ IR spectroscopy T he light-driven proton pump bacteriorhodopsin (BR) converts light energy to chemical energy by a vectorial proton transport against a membrane potential (1). In addition to belonging to the best-studied proton-permeable ion channels (2) as such and being a natural host for studying proton conducting water wires (3), BR is an important representative of the G protein-coupled seven-␣-helix receptor family (4). Thus, it comes as no surprise that this protein serves as a paradigmatic workhorse for both experiment and simulation. During its photocycle, protons are translocated to different positions within the transport channel, and a detailed dynamical picture is currently emerging for BR from the level of conformational changes to side-chain motion to individual atom displacements (5-9). In addition, biomolecular simulation strongly suggests the presence of locally mobile internal water molecules inside BR, which could easily serve as proton hosts and relays and thus establish a pathway from intracellular to extracellular space (10-12). A crucial step in this vectorial proton transfer is the actual release of a proton to the extracellular surface involving the so-called proton release group (XH). However, the very nature of XH is still a puzzling and disputed question.Whereas other initial as well as transient proton positions in BR have been quite well characterized (9), the terminal release group has withdrawn itself from identification for a long time. Recent IR spectroscopic meas...

show abstract

Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 Å resolution

Cited by 445 publications

References 36 publications

Mechanism of a proton pump analyzed with computer simulations

Mechanism of a proton pump analyzed with computer simulations

Interactions between lipids and bacterial reaction centers determined by protein crystallography

Structures and spectral signatures of protonated water networks in bacteriorhodopsin

Contact Info

Product

Resources

About