A cross-species quantitative proteomic study of salt adaptation in a halotolerant environmental isolate using 15N metabolic labelling

Proteomics

Volumn 8, Issue 11, 2008, Pages 2266-2284

  Pandhal, Jagroop ^a   Snijders, Ambrosius P L ^a   Wright, Phillip C ^a   Biggs, Catherine A ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Cross species; Cyanobacteria; Extremophile; Metabolic labelling; Salt adaptation

Indexed keywords

BACTERIAL PROTEIN; NITROGEN 15;

ARTICLE; CYANOBACTERIUM; EUHALOTHECE; ISOTOPE LABELING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; SALT TOLERANCE;

CARBON; CELL SIZE; CYANOBACTERIA; DATABASES, PROTEIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MASS SPECTROMETRY; NITROGEN ISOTOPES; POLYMERASE CHAIN REACTION; PROTEOMICS; SALTS; SOFTWARE; SPECIES SPECIFICITY;

CYANOBACTERIA; EUHALOTHECE;

EID: 43949117883     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200700398     Document Type: Article

References (67)

1. Gong, Q., Li, P., Ma, S., Indu Rupassara, S., Bohnert, H. J., Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J. 2005, 44, 826-839.
2. Kanesaki, Y., Suzuki, I., Allakhverdiev, S. I., Mikami, K., Murata, N., Salt Stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem. Biophys. Res. Commun. 2002, 290, 339-348.
3. Murata, N., Suzuki, I., Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J. Exp. Bot. 2006, 57, 235-247.
4. Pandhal, J., Wright, P. C., Biggs, C. A., A quantitative proteomic analysis of light adaptation in a globally significant marine cyanobacterium. Prochlorococcus marinus MED4. J. Proteome Res. 2007, 6, 996-1005.
5. D'Amico, S., Collins, T., Marx, J., Feller, G., Gerday, C., Psychrophilic microorganisms: challenges for life. EMBO reports 2006, 7, 385-389.
6. Liska, A. J., Shevchenko, A., Expanding the organismal scope of proteomics: cross-species protein identification by mass spectrometry and its implications. Proteomics 2003, 3, 19-28.
7. Lester, P. J., Hubbard, S. J., Comparative bioinformatic analysis of complete proteomes and protein parameters for cross-species identification in proteomics. Proteomics 2002, 2, 1392-1405.
8. Shevchenko, A., Sunyaev, S., Loboda, A., Shevchenko, A. et al., Charting the proteomes of organisms with unsequenced genomes by MALDI-quadrupole time-of-flight mass spectrometry and BLAST homology searching. Anal. Chem. 2001, 73, 1917-1926.
9. Habermann, B., Oegema, J., Sunyaev, S., Shevchenko, A., The power and the limitations of cross-species protein identification by mass spectrometry-driven sequence similarity searches. Mol. Cell Proteomics 2004, 3, 238-249.
10. Liska, A. J., Shevchenko, A., Combining mass spectrometry with database interrogation strategies in proteomics. Trends Anal. Chem. 2003, 22, 291.
11. Taylor, T. N., Taylor, E. L., The Biology and Evolution of Fossil Plants, Prentice Hall, New Jersey, New York 1993.
12. Liska, A. J., Shevchenko, A., Pick, U., Katz, A., Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol. 2004, 136, 2806-2817.
13. Sunyaev, S., Liska, A. J., Golod, A., Shevchenko, A., Shevchenko, A., MultiTag: multiple error-tolerant sequence tag search for the sequence-similarity identification of proteins by mass spectrometry. Anal. Chem. 2003, 75, 1307-1315.
14. Reed, R. H., Stewart, W. D. P., The Responses of Cyanobacteria to Salt Stress, Oxford Science Publisher, Oxford 1988.
15. Hart, B. T., Lake, P. S., Webb, J. A., Grace, M. R., Ecological risk to aquatic systems from salinity increases. Australian J. Botany 2003, 51, 689-702.
16. Parida, A. K., Das, A. B., Salt tolerance and salinity effects on plants: a review. Ecotoxicol. Environ. Saf. 2005, 60, 324-349.
17. Bryant, D. A., The cyanobacterial photosynthetic apparatus: comparisons to those of higher plants and photosynthetic bacteria. Can. Bull. Fish. Aquat. Sci. 1986.
18. Elanskaya, I. V., Karandashova, I. V., Bogachev, A. V., Hagemann, M., Functional analysis of the Na+/H+ antiporter encoding genes of the cyanobacterium Synechocystis PCC 6803. Biochemistry (Mosc.). 2002, 67, 432-440.
19. Ferjani, A., Mustardy, L., Sulpice, R., Marin, K. et al., Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol. 2003, 131, 1628-1637.
20. Hagemann, M., Jeanjean, R., Fulda, S., Havaux, M. et al., Flavodoxin accumulation contributes to enhanced cyclic electron flow around photosystem I in salt-stressed cells of Synechocystis sp. strain PCC 6803. Physiol. Plant 1999, 105, 670-678.
21. Hagemann, M., Techel, D., Rensing, L., Comparison of salt-and heat-induced alterations of protein synthesis in the cyanobacterium Synechocystis sp. PCC 6803. Arch. Microbiol. 1991, 155, 587-592.
22. Joset, F., Jeanjean, R., Hagemann, M., Dynamics of response of cyanobacteria to salt stress: deciphering the molecular events. Physiol. Plant 1996, 96, 738-744.
23. Shoumskaya, M. A., Paithoonrangsarid, K., Kanesaki, Y., Los, D. A. et al., Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in synechocystis. J. Biol. Chem. 2005, 280, 21531-21538.
24. Allen, M. M., Simple conditions for growth of unicellular blue-green algae on plates. J. Phycology 1968, 4, 1-4.
25. Huang, F., Hedman, E., Funk, C., Kieselbach, T. et al., Isolation of outer membrane of Synechocystis sp. PCC 6803 and its proteomic characterization. Mol. Cell Proteomics 2004, 3, 586-595.
26. Fulda, S., Huang, F., Nilsson, F., Hagemann, M., Norling, B., Proteomics of Synechocystis sp. strain PCC 6803: Identification of periplasmic proteins cells grown at low and high salt concentrations. Eur. J. Biochem. 2000, 267, 5900-5907.
27. Huang, F., Fulda, S., Hagemann, M., Norling, B., Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 2006, 6, 910-920.
28. Fulda, S., Mikkat, S., Huang, F., Huckauf, J. et al., Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics 2006, 6, 2733-2745.
29. Höper, D., Bernhardt, J., Hecker, M., Salt stress adaptation of Bacillus subtilis: A physiological proteomics approach. Proteomics 2006, 6, 1550-1562.
30. Snijders, A. P., de Vos, M. G., de Koning, B., Wright, P. C., A fast method for quantitative proteomics based on a combination between two-dimensional electrophoresis and 15N-metabolic labelling. Electrophoresis 2005, 26, 3191-3199.
31. Gao, X., Ren, Z., Zhao, Y., Zhang, H., Overexpression of SOD2 increases salt tolerance of Arabidopsis. Plant Physiol. 2003, 133, 1873-1881.
32. Rippka, R., Deruelles, J., Waterbury, J. B., Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 1979, 111, 1-61.
33. Mackinney, G., Absorption of light by chlorophyll solutions. J. Biol. Chem. 1941, 140, 315-322
34. Gan, C. S., Reardon, K. F., Wright, P. C., Comparison of protein and peptide prefractionation methods for the shotgun proteomic analysis of Synechocystis sp. PCC 6803. Proteomics 2005, 5, 2468-2478.
35. Perkins, D. N., Pappin, D. J. C., Creasy, D. M., Cottrell, J. S., Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20, 3551-3567.
36. Gardy, J. L., Laird, M. R., Chen, F., Rey, S. et al., PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 2005, 21, 617-623.
37. Juncker, A. S., Willenbrock, H., Von Heijne, G., Brunak, S. et al., Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 2003, 12, 1652-1662.
38. Nubel, U., Garcia-Pichel, F., Clavero, E., Muyzer, G., Matching molecular diversity and ecophysiology of benthic cyanobacteria and diatoms in communities along a salinity gradient. Environ. Microbiol. 2000, 2, 217-226.
39. Snijders, A. P., de Vos, M. G., Wright, P. C., Novel approach for peptide quantitation and sequencing based on 15N and 13C metabolic labeling. J. Proteome Re.s 2005, 4, 578-585.
40. Hagemann, M., Fulda, S., Schubert, H., DNA, RNA, and protein synthesis in the cyanobacterium Synechocystis sp. PCC 6803 adapted to different salt concentrations. Curr. Microbiol. 1994, 28, 201-207.
41. Kaneko, T., Sato, S., Kotani, H., Tanaka, A. et al., Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions (supplement). DNA Res. 1996, 3, 185-209.
42. Cagney, G., Amiri, S., Premawaradena, T., Lindo, M., Emili, A., In silico proteome analysis to facilitate proteomics experiments using mass spectrometry. Proteome Sci. 2003, 1, 5.
43. Apte, S. K., Fernandes, T., Badran, H., Ballal, A., Expression and possible role of stress-responsive proteins in Anabaena. J. Biosci. 1998, 23, 399-406.
44. Kramer, G., Rutkowska, A., Wegrzyn, R. D., Patzelt, H. et al., Functional dissection of Escherichia coli trigger factor: unraveling the function of individual domains. J. Bacteriol. 2004, 186, 3777-3784.
45. Liu, H. B., Nolla, H. A., Campbell, L., Prochlorococcus growth rate and contribution to primary production in the Equatorial and Subtropical North Pacific ocean. Aquat. Microb. Ecol. 1997, 12, 39-47.
46. Knight, H., Trewavas, A. J., Knight, M. R., Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 1997, 12, 1067-1078.
47. Scott, J., Rébeillé, F., Fletcher, J., Folic acid and folates: the feasibility for nutritional enhancement in plant foods. J. Sci. Food Agric. 2000, 80, 795-824.
48. Fischer, G., Schmid, F. X., The mechanism of protein folding. Implications of in vitro refolding models for de novo protein folding and translocation in the cell. Biochemistry 1990, 29, 2205-2212.
49. Dym, O., Mevarech, M., Sussman, J. L., Structural features that stabilize halophilic malate dehydrogenase from an Archaebacterium. Science 1995, 267, 1344-1346.
50. Frolow, F., Harel, M., Sussman, J. L., Mevarech, M., Shoham, M., Insights into protein adaptation to a saturated salt environment from the crystal structure of a halophilic 2Fe-2S ferredoxin. Nat. Struct. Mol. Biol. 1996, 3, 452.
51. Rao, J. K., Argos, P., Structural stability of halophilic proteins. Biochemistry 1981, 20, 6536-6543.
52. Ashhuby, B. A., Chemical and Process Engineering, University of Sheffield, Sheffield 2007, p. 221.
53. Zuther, E., Schubert, H., Hagemann, M., Mutation of a gene encoding a putative glycoprotease leads to reduced salt tolerance, altered pigmentation, and cyanophycin accumulation in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 1998, 180, 1715-1722.
54. Samartzidou, H., Widger, W. R., Transcriptional and posttranscriptional control of mRNA from IrtA, a light-repressed transcript in Synechococcus sp. PCC 7002. Plant Physiol. 1998, 117, 225-234.
55. Walker, G. C., The SOS Response of Escherichia coli, ASM Press, Washington D.C. 1996.
56. Domain, F., Houot, L., Chauvat, F., Cassier-Chauvat, C., Function and regulation of the cyanobacterial genes lexA, recA and ruvB: LexA is critical to the survival of cells facing inorganic carbon starvation. Mol. Microbiol. 2004, 53, 65-80.
57. Gutekunst, K., Phunpruch, S., Schwarz, C., Schuchardt, S. et al., LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator. Mol. Microbiol. 2005, 58, 810-823.
58. Oliveira, P., Lindblad, P., LexA, a transcription regulator binding in the promoter region of the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol. Letters 2005, 251, 59.
59. Schutz, K., Happe, T., Troshina, O., Lindblad, P. et al., Cyanobacterial H2 production - a comparative analysis. Planta 2004, 218, 350-359.
60. Zhu, J. K., Plant salt tolerance. Trends Plant Sci. 2001, 6, 66-71.
61. Vinnemeier, J., Kunert, A., Hagemann, M., Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC6803. FEMS Microbiol. Lett. 1998, 169, 323-330.
62. Wilkinson, M. J., Northcote, D. H., Plasma membrane ultrastructure during plant protoplast plasmolysis, isolation and wall regeneration: a freeze-fracture study. J. Cell Sci. 1980, 42, 401-415.
63. Schubert, H., Fulda, S., Hagemann, M., Effects of adaptation to different salt concentrations on photosynthesis and pigmentation of the cyanobacterium Synechocystis sp. PCC 6803 J. Plant Physiol. 1993, 142, 291-295.
64. Verma, K., Mohanty, P., Changes of the photosynthetic apparatus in Spirulina cyanobacterium by sodium stress. Z. Naturforsch. [C]. 2000, 55, 16-22.
65. Verma, K., Mohanty, P., Alterations in the structure of phycobilsomes of cyanobacterium Spirulina platensis in response to enhanced sodium level. World J. Microbiol. Biotechnol. 2000, 16, 795-798.
66. Marin, K., Kanesaki, Y., Los, D. A., Murata, N. et al., Gene expression profiling reflects physiological processes in salt acclimation of Synechocystis sp. strain PCC 6803. Plant Physiol. 2004, 136, 3290-3300.
67. Murthy, K. N. C., Vanitha, A., Rajesha, J., Swamy, M. M. et al., In vivo antioxidant activity of carotenoids from Dunaliella saline - a green microalga. Life Sci. 2005, 76, 1381.