The light-activated proton pump Bop i of the archaeon Haloquadratum walsbyi

Photochemistry and Photobiology

Volumn 88, Issue 3, 2012, Pages 690-700

  Lobasso, Simona ^a   Lopalco, Patrizia ^b   Vitale, Rita ^a   Saponetti, Matilde Sublimi ^c   Capitanio, Giuseppe ^a   Mangini, Vincenzo ^a   Milano, Francesco ^b   Trotta, Massimo ^b   Corcelli, Angela ^a,b  

^a UNIVERSITY OF BARI   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF SALERNO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PRIMER DNA; PROTON PUMP;

ARTICLE; CIRCULAR DICHROISM; ELECTROSPRAY MASS SPECTROMETRY; GEL CHROMATOGRAPHY; HALOBACTERIALES; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; KINETICS; LIGHT; METABOLISM; NUCLEOTIDE SEQUENCE; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; RADIATION EXPOSURE; REAL TIME POLYMERASE CHAIN REACTION; ULTRAVIOLET SPECTROPHOTOMETRY;

BASE SEQUENCE; CHROMATOGRAPHY, GEL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CIRCULAR DICHROISM; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HALOBACTERIACEAE; HYDROGEN-ION CONCENTRATION; KINETICS; LIGHT; PROTON PUMPS; REAL-TIME POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROPHOTOMETRY, ULTRAVIOLET;

ARCHAEA; HALOQUADRATUM WALSBYI;

EID: 84860673240     PISSN: 00318655     EISSN: 17511097     Source Type: Journal    
DOI: 10.1111/j.1751-1097.2012.01089.x     Document Type: Article

References (64)

1. Bolhuis, H., E. M. te Poele, and, F. Rodriguez-Valera, (2004) Isolation and cultivation of Walsby's square archaeon. Environ. Microbiol. 6, 1287-1291.
2. Walsby, A. E., (1980) A square bacterium. Nature 283, 69-71.
3. Burns, D. G., P. H. Janssen, T. Itoh, M. Kamekura, Z. Li, G. Jensen, F. Rodriguez-Valera, H. Bolhuis, and, M. L. Dyall-Smith, (2007) Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int. J. Syst. Evol. Microbiol. 57, 387-392.
4. Oren, A., N. Pri-El, O. Shapiro, and, N. Siboni, (2006) Buoyancy studies in natural communities of square gas-vacuolate archaea in saltern crystallizer ponds. Saline Systems 2, 4-10.
5. Burns, D. G., H. M. Camakaris, P. H. Janssen, and, M. L. Dyall-Smith, (2004) Cultivation of Walsby's square haloarchaeon. FEMS Microbiol. Lett. 238, 469-473.
6. Burns, D. G., H. M. Camakaris, P. H. Janssen, and, M. L. Dyall-Smith, (2004) Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl. Environ. Microbiol. 70, 5258-5265.
7. Oren, A., S. Duker, and, S. Ritter, (1996) The polar lipid composition of Walsby's square bacterium. FEMS Microbiol. Lett. 138, 135-140.
8. Sublimi Saponetti, M., F. Bobba, G. Salerno, A. Scarfato, A. Corcelli, and, A. Cuculo, (2011) Morphological and structural aspects of the extremely halophilic archaeon Haloquadratum walsbyi. PLoS One 6, e18653.
9. Bolhuis, H., P. Palm, A. Wende, M. Falb, M. Rampp, F. Rodriguez-Valera, F. Pfeiffer, and, D. Oesterhelt, (2006) The genome of the square archaeon Haloquadratum walsbyi: Life at the limits of water activity. BMC Genomics 7, 169-180.
10. Javor, B., C. Requadt, and, W. Stoeckenius, (1982) Box-shaped halophilic bacteria. J. Bacteriol. 151, 1532-1542.
11. Sudo, Y., K. Ihara, S. Kobayashi, D. Suzuki, H. Irieda, T. Kikukawa, H. Kandori, and, M. Homma, (2011) A microbial rhodopsin with a unique retinal composition shows both sensory rhodopsin II and bacteriorhodopsin-like properties. J. Biol. Chem. 286, 5967-5976.
12. Oesterhelt, D., and, W. Stoeckenius, (1974) Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. 31, 667-678.
13. Lopez, F., S. Lobasso, M. Colella, A. Agostiano, and, A. Corcelli, (1999) Light-dependent and biochemical properties of two different bands of bacteriorhodopsin isolated on phenyl-sepharose CL-4B. Photochem. Photobiol. 69, 599-604.
14. Dencher, N. A., and, M. P. Hein, (1982) Preparation and properties of monomeric bacteriorhodopsin. Methods Enzymol 88, 5-10.
15. Schägger, H., and, G. von Jagow, (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379.
16. Lopalco, P., S. Lobasso, F. Babudri, and, A. Corcelli, (2004) Osmotic shock stimulates de novo synthesis of two cardiolipins in an extreme halophilic archaeon. J. Lipid Res. 45, 194-201.
17. Kates, M., (1986) Techniques of lipidology. In Laboratory Techniques in Biochemistry and Molecular Biology, 2nd edn, Vol. 3 (Edited by, R. H. Burdon, and, P. H. van Knippenberg,), pp. 100-110. Elsevier, Amsterdam, The Netherlands.
18. Kano, K., and, J. H. Fendler, (1978) Pyranine as a sensitive probe for liposome interiors and surfaces. pH gradients across phospholipid vesicles. Biochim. Biophys. Acta 509, 289-299.
19. Thompson, J. D., D. G. Higgins, and, T. J. Gibson, (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalities and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
20. Oren, A., (2002) Pigments of halophilic microorganisms. In Halophilic Microorganisms and their Environments (Edited by, J. Seckbach,), pp. 173-206. Kluwer Academic Publishers, Dordrecht, The Netherlands.
21. Mukohata, Y., Y. Sugiyama, K. Ihara, and, M. Yoshida, (1988) An Australian halobacterium contains a novel proton pump retinal protein: Archaerhodopsin. Biochem. Biophys. Res. Commun. 151, 1339-1345.
22. Mukohata, Y., K. Ihara, K. Uegaki, Y. Miyashita, and, Y. Sugiyama, (1991) Australian Halobacteria and their retinal-protein ion pumps. Photochem. Photobiol. 54, 1039-1045.
23. Lukashev, E. P., R. Govindjee, M. Kono, T. G. Ebrey, Y. Sugiyama, and, Y. Mukohata, (1994) pH dependence of the absorption spectra and photochemical transformations of the archaerhodopsins. Photochem. Photobiol. 60, 69-75.
24. Li, Q., Q. Sun, W. Zhao, H. Wang, and, D. Xu, (2000) Newly isolated archaerhodopsin from a strain of Chinese halobacteria and its proton pumping behavior. Biochim. Biophys. Acta 1466, 260-266.
25. Ming, M., M. Lu, S. P. Balashov, T. G. Ebrey, Q. G. Li, and, J. D. Ding, (2006) pH dependence of light-driven proton pumping by an archaerhodopsin from Tibet: Comparison with bacteriorhodopsin. Biophys. J. 90, 3322-3332.
26. Yoshimura, K., and, T. Kouyama, (2008) Structural role of bacterioruberin in the trimeric structure of archaerhodopsin-2. J. Mol. Biol. 375, 1267-1281.
27. Ming, M., Y. Z. Wang, J. Wu, D. W. Ma, Q. G. Li, and, J. D. Ding, (2006) Triton X-100 can alter the temporal sequence of the light-driven proton pump of archaerhodopsin 4. FEBS Lett. 580, 6749-6753.
28. Garty, H., G. Klemperer, M. Eisenbach, and, S. R. Caplan, (1977) The direction of light-induced pH changes in purple membrane suspensions. Influence of pH and temperature. FEBS Lett. 81, 238-241.
29. Duschl, A., M. A. McCloskey, and, J. K. Lanyi, (1988) Functional reconstitution of halorhodopsin. Properties of halorhodopsin-containing proteoliposomes. J. Biol. Chem. 263, 17016-17022.
30. Dencher, N. A., and, M. P. Hein, (1978) Formation and properties of bacteriorhodopsin monomers in the non-ionic detergent octyl-β-d-glucoside and Triton X-100. FEBS Lett. 96, 322-326.
31. Casadio, R., H. Gutowitz, P. Mowery, M. Taylor, and, W. Stoeckenius, (1982) Light-dark adaptation of bacteriorhodopsin in triton-treated purple membrane. Biochim. Biophys. Acta 590, 13-23.
32. Druckmann, S., M. Ottolenghi, A. Pande, J. Pande, and, R. H. Callender, (1982) Acid-base equilibrium of the Schiff base in bacteriorhodopsin. Biochemistry 21, 4953-4959.
33. +-release and uptake during the photochemical cycle of bacteriorhodopsin. FEBS Lett. 208, 337-342.
34. Corcelli, A., M. Colella, G. Mascolo, F. P. Fanizzi, and, M. Kates, (2000) A novel glycolipid and phospholipid in the purple membrane. Biochemistry 39, 3318-3326.
35. Corcelli, A., (2009) The cardiolipin analogues of Archaea. Biochim. Biophys. Acta 1788, 2101-2106.
36. de Souza, L. M., M. Müller-Santos, M. Iacomini, P. A. Gorin, and, G. L. Sassaki, (2009) Positive and negative tandem mass spectrometric fingerprints of lipids from the halophilic Archaea Haloarcula marismortui. J. Lipid Res. 50, 1363-1373.
37. Dyall-Smith, M. L., F. Pfeiffer, K. Klee, P. Palm, K. Gross, S. C. Schuster, M. Rampp, and, D. Oesterhelt, (2011) Haloquadratum walsbyi: Limited diversity in a global pond. PLoS One 6, e20968.
38. Ihara, K., T. Umemura, I. Katagiri, T. Kitajima-Ihara, Y. Sugiyama, Y. Kimura, and, Y. Mukohata, (1999) Evolution of the archaeal rhodopsins: Evolution rate changes by gene duplication and functional differentiation. J. Mol. Biol. 285, 163-174.
39. -), and its coupled ATP formation. Biochim. Biophys. Acta 1188, 287-292.
40. Tateno, M., K. Ihara, and, Y. Mukohata, (1994) The novel ion pump rhodopsin from Haloarcula form a family independent from both the bacteriorhodopsin and archaerhodopsin families/tribes. Arch. Biochem. Biophys. 315, 127-132.
41. Balashov, S. P., and, J. K. Lanyi, (2007) Xanthorhodopsin: Proton pump with a carotenoid antenna. Cell. Mol. Life Sci. 64, 2323-2328.
42. Boichenko, V. A., J. M. Wang, J. Anton, J. K. Lanyi, and, S. P. Balashov, (2006) Functions of carotenoids in xanthorhodopsin and archaerhodopsin, from action spectra of photoinhibition of cell respiration. Biochim. Biophys. Acta 1757, 1649-1656.
43. Lin, T., Q. Sun, Q. Li, Y. Huang, Q. Wei, Y. Zhang, J. Hu, Z. Zhang, M. Li, and, F. Yang, (2001) Imaging bacteriorhodopsin-like molecules of claret-membranes from Tibet halobacteria xz515 by atomic force microscope. Chinese Sci. Bull. 46, 1897-1900.
44. Gibson, J. A., M. R. Miller, N. W. Davies, G. P. Neill, D. S. Nichols, and, J. K. Volkman, (2005) Unsaturated diether lipids in the psychrotrophic archaeon Halorubrum lacusprofundi. Syst. Appl. Microbiol. 28, 19-26.
45. 4 of an allyl ether choline-phospholipid, archaetidylcholine, from the hyperthermophilic methanoarchaeon Methanopyrus kandleri. Archaea. 1, 123-131.
46. Gonthier, I., M. N. Rager, P. Metzger, J. Guezennec, and, C. Largeau, (2001) A di-O-dihydrogeranylgeranyl glycerol from Thermococcus S 557, a novel ether lipid, and likely intermediate in the biosynthesis of diethers in Archaea. Tetrahedron Lett. 42, 2795-2797.
47. Angelini, R., F. Babudri, S. Lobasso, and, A. Corcelli, (2011) MALDI-TOF/MS analysis of archaebacterial lipids in lyophilized membranes dry-mixed with 9-aminoacridine. J. Lipid Res. 51, 2818-2825.
48. Corcelli, A., V. M. T. Lattanzio, P. Papadia, and, F. P. Fanizzi, (2002) Lipid/protein stoichiometries in a crystalline biological membrane: NMR quantitative analysis of the lipid extract of the purple membrane. J. Lipid Res. 43, 132-140.
49. Sprott, G. D., S. Laroque, N. Cadotte, C. J. Dicaire, M. McGee, and, J. I. Brisson, (2003) Novel polar lipids of halophilic eubacterium Planococcus H8 and archaeon Haloferax volcanii. Biochim. Biophys. Acta 1633, 179-188.
50. Lattanzio, V. M. T., A. Corcelli, G. Mascolo, and, A. Oren, (2002) Presence of two novel cardiolipins in the halophilic archaeal community in the crystallizer brines from the salterns of Margherita di Savoia (Italy) and Eilat (Israel). Extremophiles 6, 437-444.
51. Lobasso, S., P. Lopalco, G. Mascolo, and, A. Corcelli, (2008) Lipids of the ultra-thin square halophilic archaeon Haloquadratum walsbyi. Archaea 2, 177-183.
52. Mileykovskaya, E., M. Zhang, and, W. Dowhan, (2004) Cardiolipin in energy transducing membranes. Biochemistry (Mosc) 70, 154-158.
53. Corcelli, A., S. Lobasso, M. Sublimi Saponetti, A. Leopold, and, N. A. Dencher, (2007) Glycocardiolipin modulates the surface interaction of the proton pumped by bacteriorhodopsin in purple membrane preparations. Biochim. Biophys. Acta 1768, 2157-2163.
54. Corcelli, A., S. Lobasso, L. L. Palese, M. Sublimi Saponetti, and, S. Papa, (2007) Cardiolipin is associated with the terminal oxidase of an extremely halophilic archaeon. Biochim. Biophys. Res. Commun. 354, 795-801.
55. Schlame, M., (2008) Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes. J. Lipid Res. 49, 1607-1620.
56. Haines, T. H., (2009) A new look at cardiolipin. Biochim. Biophys. Acta 1788, 1997-2002.
57. Wilkinson, S. G., (1988) Gram-negative bacteria. In Microbial Lipids (Edited by, C. Ratledge, and, S. G. Wilkinson,), pp. 299-488. Academic Press, London, UK.
58. O'Leary, W. M., and, S. G. Wilkinson, (1988) Gram-positive bacteria. In Microbial Lipids (Edited by, C. Ratledge, and, S. G. Wilkinson,), pp. 117-201. Academic Press, London, UK.
59. Lusk, J. E., and, E. P. Kennedy, (1972) Altered phospholipid metabolism in a sodium sensitive mutant of Escherichia coli. J. Bacteriol. 109, 1034-1046.
60. Okabe, A., Y. Hirai, H. Hayashi, and, Y. Kanemasa, (1990) Alteration in phospholipid composition of Staphylococcus aureus during formation of autoplast. Biochim. Biophys. Acta 617, 28-35.
61. Lobasso, S., P. Lopalco, V. M. T. Lattanzio, and, A. Corcelli, (2003) Osmotic shock induces the presence of glycocardiolipin in the purple membrane of Halobacterium salinarum. J. Lipid Res. 44, 2120-2126.
62. Catucci, L., N. Depalo, V. M. T. Lattanzio, A. Agostiano, and, A. Corcelli, (2004) Neo-synthesis of cardiolipin in Rhodobacter sphaeroides under osmotic stress. Biochemistry 43, 15066-15072.
63. De Leo, V., L. Catucci, A. Ventrella, F. Milano, A. Agostiano, and, A. Corcelli, (2009) Cardiolipin increases in chromatophores isolated from Rhodobacter sphaeroides after osmotic stress: Structural and functional roles. J. Lipid Res. 50, 256-264.
64. Catucci, L., V. M. T. Lattanzio, S. Lobasso, A. Agostiano, and, A. Corcelli, (2004) Role of endogenous lipids in the chromophore regeneration of bacteriorhodopsin. Bioelectrochemistry 63, 111-115.