Proteogenomic insights into salt tolerance by a halotolerant alpha-proteobacterium isolated from an Andean saline spring

Journal of Proteomics

Volumn 97, Issue , 2014, Pages 36-47

  Rubiano Labrador, Carolina ^a,b   Bland, Céline ^c   Miotello, Guylaine ^c   Guérin, Philippe ^c   Pible, Olivier ^c   Baena, Sandra ^a,b   Armengaud, Jean ^c  

^a PONTIFICIA UNIVERSIDAD JAVERIANA   (Colombia)

^b Colombian Center for Genomics and Bioinformatics of Extreme Environments ^*  (Colombia)

^c DIF   (France)

Author keywords

Alphaproteobacteria; Draft genome; Halotolerance; Proteogenomics; Rhodospirillaceae

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; GLUTAMIC ACID; HEAT SHOCK PROTEIN; PROTEINASE; PROTEOME; SODIUM CHLORIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CRGA; UNCLASSIFIED DRUG; PROTEIN;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM CULTURE; BACTERIUM ISOLATION; CELL GROWTH; GENE IDENTIFICATION; GENE SEQUENCE; GENOMICS; HYPEROSMOTIC STRESS; NONHUMAN; OPEN READING FRAME; OSMOLARITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEOMICS; RHODOSPIRILLACEAE; SALINITY; SALT TOLERANCE; TANDEM MASS SPECTROMETRY; TISTLIA CONSOTENSIS; TRANSCRIPTION REGULATION; ALPHAPROTEOBACTERIA; ANIMAL CELL; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; OSMOREGULATION; PROTEIN DATABASE; PROTEIN METABOLISM; SOLUTE; SPRING;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); PROTEOBACTERIA; RHODOSPIRILLACEAE;

ALPHAPROTEOBACTERIA; DRAFT GENOME; HALOTOLERANCE; PROTEOGENOMICS; RHODOSPIRILLACEAE;

ADAPTATION, PHYSIOLOGICAL; ALPHAPROTEOBACTERIA; BACTERIAL PROTEINS; NATURAL SPRINGS; OPEN READING FRAMES; PROTEOME; SODIUM CHLORIDE; WATER MICROBIOLOGY;

EID: 84892861522     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.05.020     Document Type: Article

References (72)

1. Ventosa A., Nieto J.J., Oren A. Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 1998, 62:504-544.
2. Oren A. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 2008, 4:2.
3. Roesser M., Muller V. Osmoadaptation in bacteria and archaea: common principles and differences. Environ Microbiol 2001, 3:743-754.
4. Coker J.A., DasSarma P., Kumar J., Muller J.A., DasSarma S. Transcriptional profiling of the model Archaeon Halobacterium sp. NRC-1: responses to changes in salinity and temperature. Saline Syst 2007, 3:6.
5. Leuko S., Raftery M.J., Burns B.P., Walter M.R., Neilan B.A. Global protein-level responses of Halobacterium salinarum NRC-1 to prolonged changes in external sodium chloride concentrations. J Proteome Res 2009, 8:2218-2225.
6. Bidle K.A., Kirkland P.A., Nannen J.L., Maupin-Furlow J.A. Proteomic analysis of Haloferax volcanii reveals salinity-mediated regulation of the stress response protein PspA. Microbiology 2008, 154:1436-1443.
7. Feng de Q., Yang L.F., Lu W.D., Yang S.S. Analysis of protein expression profiles of Halobacillus dabanensis D-8T under optimal and high salinity conditions. Curr Microbiol 2007, 54:20-26.
8. Feng de Q., Zhang B., Lu W.D., Yang S.S. Protein expression analysis of Halobacillus dabanensis D-8T subjected to salt shock. J Microbiol 2006, 44:369-374.
9. Gu Z.J., Wang L., Le Rudulier D., Zhang B., Yang S.S. Characterization of the glycine betaine biosynthetic genes in the moderately halophilic bacterium Halobacillus dabanensis D-8(T). Curr Microbiol 2008, 57:306-311.
10. Oren A., Larimer F., Richardson P., Lapidus A., Csonka L.N. How to be moderately halophilic with broad salt tolerance: clues from the genome of Chromohalobacter salexigens. Extremophiles 2005, 9:275-279.
11. Canovas D., Vargas C., Csonka L.N., Ventosa A., Nieto J.J. Osmoprotectants in Halomonas elongata: high-affinity betaine transport system and choline-betaine pathway. J Bacteriol 1996, 178:7221-7226.
12. Canovas D., Vargas C., Kneip S., Moron M.J., Ventosa A., Bremer E., et al. Genes for the synthesis of the osmoprotectant glycine betaine from choline in the moderately halophilic bacterium Halomonas elongata DSM 3043, USA. Microbiology 2000, 146(Pt. 2):455-463.
13. Lamark T., Kaasen I., Eshoo M.W., Falkenberg P., McDougall J., Strom A.R. DNA sequence and analysis of the bet genes encoding the osmoregulatory choline-glycine betaine pathway of Escherichia coli. Mol Microbiol 1991, 5:1049-1064.
14. Boch J., Kempf B., Schmid R., Bremer E. Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes. J Bacteriol 1996, 178:5121-5129.
15. Duche O., Tremoulet F., Glaser P., Labadie J. Salt stress proteins induced in Listeria monocytogenes. Appl Environ Microbiol 2002, 68:1491-1498.
16. Rosenstein R., Futter-Bryniok D., Gotz F. The choline-converting pathway in Staphylococcus xylosus C2A: genetic and physiological characterization. J Bacteriol 1999, 181:2273-2278.
17. Osteras M., Boncompagni E., Vincent N., Poggi M.C., Le Rudulier D. Presence of a gene encoding choline sulfatase in Sinorhizobium meliloti bet operon: choline-O-sulfate is metabolized into glycine betaine. Proc Natl Acad Sci U S A 1998, 95:11394-11399.
18. Fan F., Ghanem M., Gadda G. Cloning, sequence analysis, and purification of choline oxidase from Arthrobacter globiformis: a bacterial enzyme involved in osmotic stress tolerance. Arch Biochem Biophys 2004, 421:149-158.
19. Zhang G.I., Hwang C.Y., Cho B.C. Thalassobaculum litoreum gen. nov., sp. nov., a member of the family Rhodospirillaceae isolated from coastal seawater. Int J Syst Evol Microbiol 2008, 58:479-485.
20. Urios L., Michotey V., Intertaglia L., Lesongeur F., Lebaron P. Nisaea denitrificans gen. nov., sp. nov. and Nisaea nitritireducens sp. nov., two novel members of the class Alphaproteobacteria from the Mediterranean Sea. Int J Syst Evol Microbiol 2008, 58:2336-2341.
21. Lopez-Lopez A., Pujalte M.J., Benlloch S., Mata-Roig M., Rossello-Mora R., Garay E., et al. Thalassospira lucentensis gen. nov., sp. nov., a new marine member of the alpha-Proteobacteria. Int J Syst Evol Microbiol 2002, 52:1277-1283.
22. Imhoff J.F., Petri R., Suling J. Reclassification of species of the spiral-shaped phototrophic purple non-sulfur bacteria of the alpha-Proteobacteria: description of the new genera Phaeospirillum gen. nov., Rhodovibrio gen. nov., Rhodothalassium gen. nov. and Roseospira gen. nov. as well as transfer of Rhodospirillum fulvum to Phaeospirillum fulvum comb. nov., of Rhodospirillum molischianum to Phaeospirillum molischianum comb. nov., of Rhodospirillum salinarum to Rhodovibrio salexigens. Int J Syst Bacteriol 1998, 48(Pt. 3):793-798.
23. Lai Q., Yuan J., Gu L., Shao Z. Marispirillum indicum gen. nov., sp. nov., isolated from a deep-sea environment. Int J Syst Evol Microbiol 2009, 59:1278-1281.
24. Choi D.H., Hwang C.Y., Cho B.C. Pelagibius litoralis gen. nov., sp. nov., a marine bacterium in the family Rhodospirillaceae isolated from coastal seawater. Int J Syst Evol Microbiol 2009, 59:818-823.
25. Yoon J.H., Kang S.J., Park S., Oh T.K. Caenispirillum bisanense gen. nov., sp. nov., isolated from sludge of a dye works. Int J Syst Evol Microbiol 2007, 57:1217-1221.
26. Coenye T., Goris J., Spilker T., Vandamme P., LiPuma J.J. Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinus limosus gen. nov., sp. nov. J Clin Microbiol 2002, 40:2062-2069.
27. Yamada K., Fukuda W., Kondo Y., Miyoshi Y., Atomi H., Imanaka T. Constrictibacter antarcticus gen. nov., sp. nov., a cryptoendolithic micro-organism from Antarctic white rock. Int J Syst Evol Microbiol 2011, 61:1973-1980.
28. Diaz-Cardenas C., Patel B.K., Baena S. Tistlia consotensis gen. nov., sp. nov., an aerobic, chemoheterotrophic, free-living, nitrogen-fixing alphaproteobacterium, isolated from a Colombian saline spring. Int J Syst Evol Microbiol 2010, 60:1437-1443.
29. Armengaud J. Proteogenomics and systems biology: quest for the ultimate missing parts. Expert Rev Proteomics 2010, 7:65-77.
30. Armengaud J. Microbiology and proteomics, getting the best of both worlds!. Environ Microbiol 2013, 15:12-23.
31. Armengaud J. A perfect genome annotation is within reach with the proteomics and genomics alliance. Curr Opin Microbiol 2009, 12:292-300.
32. Clair G., Roussi S., Armengaud J., Duport C. Expanding the known repertoire of virulence factors produced by Bacillus cereus through early secretome profiling in three redox conditions. Mol Cell Proteomics 2010, 9:1486-1498.
33. de Groot A., Dulermo R., Ortet P., Blanchard L., Guerin P., Fernandez B., et al. Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet 2009, 5:e1000434.
34. Dedieu A., Gaillard J.C., Pourcher T., Darrouzet E., Armengaud J. Revisiting iodination sites in thyroglobulin with an organ-oriented shotgun strategy. J Biol Chem 2011, 286:259-269.
35. Armengaud J., Bland C., Christie-Oleza J., Miotello M. Microbial proteogenomics, gaining ground with the avalanche of genome sequences. J Bacteriol Parasitol 2011, S3.
36. Christie-Oleza J.A., Fernandez B., Nogales B., Bosch R., Armengaud J. Proteomic insights into the lifestyle of an environmentally relevant marine bacterium. ISME J 2012, 6:124-135.
37. Dupierris V., Masselon C., Court M., Kieffer-Jaquinod S., Bruley C. A toolbox for validation of mass spectrometry peptides identification and generation of database: IRMa. Bioinformatics 2009, 25:1980-1981.
38. Cote R.G., Griss J., Dianes J.A., Wang R., Wright J.C., van den Toorn H.W., et al. The PRoteomics IDEntification (PRIDE) Converter 2 Framework: An Improved Suite of Tools to Facilitate Data Submission to the PRIDE Database and the ProteomeXchange Consortium. Mol Cell Proteomics 2012, 11:1682-1689.
39. Carvalho P.C., Fischer J.S., Chen E.I., Yates J.R., Barbosa V.C. PatternLab for proteomics: a tool for differential shotgun proteomics. BMC Bioinformatics 2008, 9:316.
40. Zivanovic Y., Armengaud J., Lagorce A., Leplat C., Guerin P., Dutertre M., et al. Genome analysis and genome-wide proteomics of Thermococcus gammatolerans, the most radioresistant organism known amongst the Archaea. Genome Biol 2009, 10:R70.
41. Franceschini A., Szklarczyk D., Frankild S., Kuhn M., Simonovic M., Roth A., et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 2013, 41:D808-D815.
42. Kennedy S.P., Ng W.V., Salzberg S.L., Hood L., DasSarma S. Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res 2001, 11:1641-1650.
43. Paul S., Bag S.K., Das S., Harvill E.T., Dutta C. Molecular signature of hypersaline adaptation: insights from genome and proteome composition of halophilic prokaryotes. Genome Biol 2008, 9:R70.
44. Greub G., Kebbi-Beghdadi C., Bertelli C., Collyn F., Riederer B.M., Yersin C., et al. High throughput sequencing and proteomics to identify immunogenic proteins of a new pathogen: the dirty genome approach. PLoS One 2009, 4:e8423.
45. Gautier V., Mouton-Barbosa E., Bouyssie D., Delcourt N., Beau M., Girard J.P., et al. Label-free quantification and shotgun analysis of complex proteomes by one-dimensional SDS-PAGE/NanoLC-MS: evaluation for the large scale analysis of inflammatory human endothelial cells. Mol Cell Proteomics 2012, 11:527-539.
46. Maguire M., Coates A.R., Henderson B. Chaperonin 60 unfolds its secrets of cellular communication. Cell Stress Chaperones 2002, 7:317-329.
47. Dorman C.J., Deighan P. Regulation of gene expression by histone-like proteins in bacteria. Curr Opin Genet Dev 2003, 13:179-184.
48. Toueille M., Mirabella B., Guerin P., Bouthier de la Tour C., Boisnard S., Nguyen H.H., et al. A comparative proteomic approach to better define Deinococcus nucleoid specificities. J Proteomics 2012, 75:2588-2600.
49. Kurtz D.M. Avoiding high-valent iron intermediates: superoxide reductase and rubrerythrin. J Inorg Biochem 2006, 100:679-693.
50. Flohe L. Changing paradigms in thiology from antioxidant defense toward redox regulation. Methods Enzymol 2010, 473:1-39.
51. Shukla H.D. Proteomic analysis of acidic chaperones, and stress proteins in extreme halophile Halobacterium NRC-1: a comparative proteomic approach to study heat shock response. Proteome Sci 2006, 4:6.
52. Kapatai G., Large A., Benesch J.L., Robinson C.V., Carrascosa J.L., Valpuesta J.M., et al. All three chaperonin genes in the archaeon Haloferax volcanii are individually dispensable. Mol Microbiol 2006, 61:1583-1597.
53. Franzetti B., Schoehn G., Ebel C., Gagnon J., Ruigrok R.W., Zaccai G. Characterization of a novel complex from halophilic archaebacteria, which displays chaperone-like activities in vitro. J Biol Chem 2001, 276:29906-29914.
54. Ambily Nath I.V., Loka Bharathi P.A. Diversity in transcripts and translational pattern of stress proteins in marine extremophiles. Extremophiles 2011, 15:129-153.
55. Mojica F.J., Cisneros E., Ferrer C., Rodriguez-Valera F., Juez G. Osmotically induced response in representatives of halophilic prokaryotes: the bacterium Halomonas elongata and the archaeon Haloferax volcanii. J Bacteriol 1997, 179:5471-5481.
56. Kuo Y.P., Thompson D.K., St Jean A., Charlebois R.L., Daniels C.J. Characterization of two heat shock genes from Haloferax volcanii: a model system for transcription regulation in the Archaea. J Bacteriol 1997, 179:6318-6324.
57. Kavanagh K.L., Jornvall H., Persson B., Oppermann U. Medium- and short-chain dehydrogenase/reductase gene and protein families: the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol Life Sci 2008, 65:3895-3906.
58. Maddocks S.E., Oyston P.C. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 2008, 154:3609-3623.
59. Banos R.C., Martinez J., Polo C., Madrid C., Prenafeta A., Juarez A. The yfeR gene of Salmonella enterica serovar Typhimurium encodes an osmoregulated LysR-type transcriptional regulator. FEMS Microbiol Lett 2011, 315:63-71.
60. Lacroix J.M., Bohin J.P. Osmoregulated periplasmic glucan polymerization requires constant protein synthesis in Escherichia coli. Curr Microbiol 2010, 61:396-400.
61. Lequette Y., Rollet E., Delangle A., Greenberg E.P., Bohin J.P. Linear osmoregulated periplasmic glucans are encoded by the opgGH locus of Pseudomonas aeruginosa. Microbiology 2007, 153:3255-3263.
62. Page F., Altabe S., Hugouvieux-Cotte-Pattat N., Lacroix J.M., Robert-Baudouy J., Bohin J.P. Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity. J Bacteriol 2001, 183:3134-3141.
63. Jain S., Goldberg M.B. Requirement for YaeT in the outer membrane assembly of autotransporter proteins. J Bacteriol 2007, 189:5393-5398.
64. Kramer R. Bacterial stimulus perception and signal transduction: response to osmotic stress. Chem Rec 2010, 10:217-229.
65. Mulligan C., Fischer M., Thomas G.H. Tripartite ATP-independent periplasmic (TRAP) transporters in bacteria and archaea. FEMS Microbiol Rev 2011, 35:68-86.
66. Walmsley A.R., Shaw J.G., Kelly D.J. The mechanism of ligand binding to the periplasmic C4-dicarboxylate binding protein (DctP) from Rhodobacter capsulatus. J Biol Chem 1992, 267:8064-8072.
67. Bolhuis A. Protein transport in the halophilic archaeon Halobacterium sp. NRC-1: a major role for the twin-arginine translocation pathway?. Microbiology 2002, 148:3335-3346.
68. Rose R.W., Bruser T., Kissinger J.C., Pohlschroder M. Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol Microbiol 2002, 45:943-950.
69. Nanduri B., Lawrence M.L., Vanguri S., Pechan T., Burgess S.C. Proteomic analysis using an unfinished bacterial genome: the effects of subminimum inhibitory concentrations of antibiotics on Mannheimia haemolytica virulence factor expression. Proteomics 2005, 5:4852-4863.
70. Sun J., Wang W., Hundertmark C., Zeng A.P., Jahn D., Deckwer W.D. A protein database constructed from low-coverage genomic sequence of Bacillus megaterium and its use for accelerated proteomic analysis. J Biotechnol 2006, 124:486-495.
71. Junqueira M., Spirin V., Balbuena T.S., Thomas H., Adzhubei I., Sunyaev S., et al. Protein identification pipeline for the homology-driven proteomics. J Proteomics 2008, 71:346-356.
72. Samyn B., Sergeant K., Memmi S., Debyser G., Devreese B., Van Beeumen J. MALDI-TOF/TOF de novo sequence analysis of 2-D PAGE-separated proteins from Halorhodospira halophila, a bacterium with unsequenced genome. Electrophoresis 2006, 27:2702-2711.