Light-independent phospholipid scramblase activity of bacteriorhodopsin from Halobacterium salinarum
Abstract
The retinylidene protein bacteriorhodopsin (BR) is a heptahelical light-dependent proton pump found in the purple membrane of the archaeon Halobacterium salinarum. We now show that when reconstituted into large unilamellar vesicles, purified BR trimers exhibit light-independent lipid scramblase activity, thereby facilitating transbilayer exchange of phospholipids between the leaflets of the vesicle membrane at a rate >10,000 per trimer per second. This activity is comparable to that of recently described scramblases including bovine rhodopsin and fungal TMEM16 proteins. Specificity tests reveal that BR scrambles fluorescent analogues of common phospholipids but does not transport a glycosylated diphosphate isoprenoid lipid. In silico analyses suggest that membrane-exposed polar residues in transmembrane helices 1 and 2 of BR may provide the molecular basis for lipid translocation by coordinating the polar head-groups of transiting phospholipids. Consistent with this possibility, extensive coarse-grained molecular dynamics simulations of a BR trimer in an explicit phospholipid membrane revealed water penetration along transmembrane helix 1 with the cooperation of a polar residue (Y147 in transmembrane helix 5) in the adjacent protomer. Finally, these results suggest that the lipid translocation pathway may lie at or near the interface of the protomers of a BR trimer.
- Authors:
-
- Weill Cornell Medical College, New York, NY (United States). Dept. of Biochemistry
- Univ. of Toronto, ON (Canada). Dept. of Biochemistry
- Univ. of Bern (Switzerland). Inst. of Biochemistry and Molecular Medicine
- Univ. of Toronto, ON (Canada). Dept. of Biochemistry and Dept. of Molecular Genetics
- Weill Cornell Medical College, New York, NY (United States). Dept. of Physiology and Biophysics, and Inst. for Computational Biomedicine
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1490733
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Scientific Reports
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2045-2322
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Verchère, Alice, Ou, Wei-Lin, Ploier, Birgit, Morizumi, Takefumi, Goren, Michael A., Bütikofer, Peter, Ernst, Oliver P., Khelashvili, George, and Menon, Anant K. Light-independent phospholipid scramblase activity of bacteriorhodopsin from Halobacterium salinarum. United States: N. p., 2017.
Web. doi:10.1038/s41598-017-09835-5.
Verchère, Alice, Ou, Wei-Lin, Ploier, Birgit, Morizumi, Takefumi, Goren, Michael A., Bütikofer, Peter, Ernst, Oliver P., Khelashvili, George, & Menon, Anant K. Light-independent phospholipid scramblase activity of bacteriorhodopsin from Halobacterium salinarum. United States. https://doi.org/10.1038/s41598-017-09835-5
Verchère, Alice, Ou, Wei-Lin, Ploier, Birgit, Morizumi, Takefumi, Goren, Michael A., Bütikofer, Peter, Ernst, Oliver P., Khelashvili, George, and Menon, Anant K. Fri .
"Light-independent phospholipid scramblase activity of bacteriorhodopsin from Halobacterium salinarum". United States. https://doi.org/10.1038/s41598-017-09835-5. https://www.osti.gov/servlets/purl/1490733.
@article{osti_1490733,
title = {Light-independent phospholipid scramblase activity of bacteriorhodopsin from Halobacterium salinarum},
author = {Verchère, Alice and Ou, Wei-Lin and Ploier, Birgit and Morizumi, Takefumi and Goren, Michael A. and Bütikofer, Peter and Ernst, Oliver P. and Khelashvili, George and Menon, Anant K.},
abstractNote = {The retinylidene protein bacteriorhodopsin (BR) is a heptahelical light-dependent proton pump found in the purple membrane of the archaeon Halobacterium salinarum. We now show that when reconstituted into large unilamellar vesicles, purified BR trimers exhibit light-independent lipid scramblase activity, thereby facilitating transbilayer exchange of phospholipids between the leaflets of the vesicle membrane at a rate >10,000 per trimer per second. This activity is comparable to that of recently described scramblases including bovine rhodopsin and fungal TMEM16 proteins. Specificity tests reveal that BR scrambles fluorescent analogues of common phospholipids but does not transport a glycosylated diphosphate isoprenoid lipid. In silico analyses suggest that membrane-exposed polar residues in transmembrane helices 1 and 2 of BR may provide the molecular basis for lipid translocation by coordinating the polar head-groups of transiting phospholipids. Consistent with this possibility, extensive coarse-grained molecular dynamics simulations of a BR trimer in an explicit phospholipid membrane revealed water penetration along transmembrane helix 1 with the cooperation of a polar residue (Y147 in transmembrane helix 5) in the adjacent protomer. Finally, these results suggest that the lipid translocation pathway may lie at or near the interface of the protomers of a BR trimer.},
doi = {10.1038/s41598-017-09835-5},
journal = {Scientific Reports},
number = 1,
volume = 7,
place = {United States},
year = {Fri Aug 25 00:00:00 EDT 2017},
month = {Fri Aug 25 00:00:00 EDT 2017}
}
Web of Science
Figures / Tables:
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