Proteomic insights into cold adaptation of psychrotrophic and mesophilic Acidithiobacillus ferrooxidans strains

Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology

Volumn 100, Issue 2, 2011, Pages 259-277

  Mykytczuk, Nadia C S ^a   Trevors, Jack T ^b   Foote, Simon J ^d   Leduc, Leo G ^e   Ferroni, Garry D ^c   Twine, Susan M ^d  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

^c NORTHERN ONTARIO SCHOOL OF MEDICINE   (Canada)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^e LAURENTIAN UNIVERSITY   (Canada)

Author keywords

Acidithiobacillus ferrooxidans; Adaptation; Bacteria; Cold temperatures; Proteome; Stress

Indexed keywords

ABC TRANSPORTER; BACTERIAL PROTEIN; CAPSULE POLYSACCHARIDE TRANSPORT PROTEIN; CARRIER PROTEIN; CHAPERONE; CHAPERONIN; IRON; PROTEIN AHPC TSA; PROTEIN SECB; PROTEIN SURA; PROTEIN TIG; RUSTICYANIN; UNCLASSIFIED DRUG;

ACIDITHIOBACILLUS FERROOXIDANS; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOINFORMATICS; COLD ACCLIMATIZATION; COLD CLIMATE; COLD TOLERANCE; IRON METABOLISM; LOW TEMPERATURE; MEMBRANE TRANSPORT; MESOPHILIC BACTERIUM; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; STRAIN DIFFERENCE;

ACIDITHIOBACILLUS; ADAPTATION, PHYSIOLOGICAL; AZURIN; BACTERIAL PROTEINS; CARBON; COLD TEMPERATURE; COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; IRON; MEMBRANE TRANSPORT PROTEINS; MOLECULAR CHAPERONES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHYLOGENY; PROTEIN FOLDING; PROTEIN ISOFORMS; PROTEOME;

ACIDITHIOBACILLUS FERROOXIDANS;

EID: 79960708206     PISSN: 00036072     EISSN: 15729699     Source Type: Journal    
DOI: 10.1007/s10482-011-9584-z     Document Type: Article

References (61)

1. RC Allen 1980 Rapid isoelectric focusing and detection of nanogram amounts of proteins from body tissues and fluids Electrophoresis I 32 37 10.1002/elps.1150010107 (Pubitemid 10002205)
2. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389 3402 9254694 10.1093/nar/25.17.3389 1:CAS:528:DyaK2sXlvFyhu7w%3D (Pubitemid 27359211)
3. AM Amaro D Chamorro M Seeger R Arredondo I Peirano CA Jerez 1991 Effect of external pH perturbations on in vivo protein synthesis by the acidophilic bacterium Thiobacillus ferrooxidans J Bacteriol 173 2 910 915 1987171 1:CAS:528:DyaK3MXnvVCmsA%3D%3D
4. A Amouric C Brochier-Armanet DB Johnson V Bonnefoy KB Hallberg 2011 Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways Microbiology 157 111 122 20884692 10.1099/mic.0.044537-0 1:CAS:528:DC%2BC3MXhtlCgtLo%3D
5. M Barreto E Jedlicki DS Holmes 2005 Identification of a gene cluster for the formation of extracellular polysaccharide precursors in the chemolithoautotroph Acidithiobacillus ferrooxidans Appl Environ Microbiol 71 6 2902 2909 15932984 10.1128/AEM.71.6.2902-2909.2005 1:CAS:528: DC%2BD2MXlt1Okt78%3D (Pubitemid 40807193)
6. Beal C, Fonseca F, Corrieu G (2001) Resistance to freezing and frozen storage of Streptococcus thermophilus is related to membrane fatty acid composition. J Dairy Sci 84:2347-2356 (Pubitemid 33613052)
7. PW Bergholz C Bakermans JM Tiedje 2009 Psychrobacter arcticus 273-4 uses resource efficiency and molecular motion adaptations for subzero temperature growth J Bacteriol 191 2340 2352 19168616 10.1128/JB.01377-08 1:CAS:528:DC%2BD1MXjvVOgsL0%3D
8. NH Bergman KD Passalacqua PC Hanna ZS Qin 2007 Operon prediction for sequenced bacterial genomes without experimental information Appl Environ Microbiol 73 3 846 854 17122389 10.1128/AEM.01686-06 1:CAS:528: DC%2BD2sXltlalsLw%3D (Pubitemid 46233501)
9. AN Bittner A Foltz V Oke 2007 Only one of five groEL genes is required for viability and successful symbiosis in Sinorhizobium meliloti J Bacteriol 189 5 1884 1889 17158666 10.1128/JB.01542-06 1:CAS:528:DC%2BD2sXitl2hsrg%3D (Pubitemid 46446151)
10. P Bouchal Z Zdrahal S Helanova O Janiczek KB Hallberg M Mandl 2006 Proteomic and bioinformatics analysis of iron- and sulfur-oxydizing Acidithiobacillus ferrooxidans using immobilized pH gradient and mass spectrometry Proteomics 6 4278 4285 16807941 10.1002/pmic.200500719 1:CAS:528:DC%2BD28XovVKqt7k%3D (Pubitemid 44277030)
11. E Cabiscol J Tamarit J Ros 2000 Oxidative stress in bacteria and protein damage by reactive oxygen species Int Microbiol 3 3 8 10963327 1:CAS:528:DC%2BD3cXksVCnur0%3D
12. E Cascales R Lloubès JN Sturgis 2008 The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB Mol Microbiol 42 3 795 807 10.1046/j.1365-2958.2001.02673.x
13. I Cases DW Ussery V De Lorenzo 2003 The σ54 regulon (sigmulon) of Pseudomonas putida Environ Microbiol 5 12 1281 1293 14641574 10.1111/j.1462-2920.2003.00528.x 1:CAS:528:DC%2BD2cXkslKnsQ%3D%3D (Pubitemid 38038940)
14. A Chi L Valenzuela S Bears A Mackey J Shabanowitz DF Hunt CA Jerez 2007 Periplasmic proteins of the extremophile Acidithiobacillus ferrooxidans Mol Cell Proteomics 6 2239 2251 17911085 10.1074/mcp.M700042-MCP200 1:CAS:528: DC%2BD1cXksF2hsQ%3D%3D
15. JC Cox DH Boxer 1978 The purification and some properties of rusticyanin, a blue copper protein involved in iron (II) oxidation from Thiobacillus ferrooxidans Biochem J 174 497 502 708402 1:CAS:528:DyaE1MXpvVOksw%3D%3D (Pubitemid 8403657)
16. S D'Amico T Collins J-C Marx G Feller C Gerday 2006 Psychophilic microorganisms: challenges for life EMBO reports 7 4 385 389 16585939 10.1038/sj.embor.7400662
17. M Dopson A-K Halinen N Rahunen B Ozkaya E Sahinkaya AH Kaksonen EB Lindstom JA Puhakka 2007 Mineral and iron oxidation at low temperatures by pure and mixed cultures of acidophilic microorganisms Biotechnol Bioeng 97 5 1205 1215 17187443 10.1002/bit.21312 1:CAS:528:DC%2BD2sXnvFagtr0%3D (Pubitemid 47195317)
18. MJ Fath R Kolter 1993 ABC transporters: bacterial exporters Microbiol Rev 57 4 995 1017 8302219 1:CAS:528:DyaK2cXnt12msw%3D%3D (Pubitemid 24004512)
19. AP Felício O Garcia Jr MC Bertolini LMM Ottoboni MTM Novo 2003 The effects of copper ions on the synthesis of periplasmic and membrane proteins in Acidithiobacillus ferrooxidans as analyzed by SDS-PAGE and 2D-PAGE Hydrometallurgy 71 1-2 165 171 10.1016/S0304-386X(03)00153-1
20. GD Ferroni LG Leduc M Todd 1986 Isolation and temperature characterization of psychrotrophic strains of Thiobacillus ferrooxidans from the environment of a uranium mine J Gen App Microbiol 32 169 175 10.2323/jgam.32.169 1:CAS:528:DyaL28XmtVGqt7c%3D
21. M Furuki N Tanaka T Hiyama H Nakamoto 1996 Cloning, characterization and functional analysis of groEL-like gene from thermophilic cyanobacterium Synechococcus vulcanus, which does not form an operon with groES Biochim Biophys Acta 1294 106 110 8645726 10.1016/0167-4838(96)00037-4 (Pubitemid 26178831)
22. JL Gardy MR Laird F Chen S Rey CJ Walsh M Ester FSL Brinkman 2005 PSORTb v20: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis Bioinformatics 21 5 617 623 15501914 10.1093/bioinformatics/bti057 1:CAS:528:DC%2BD2MXhslSltb8%3D (Pubitemid 40424787)
23. WG Haldenwang 1995 The sigma factors of Bacillus subtilis Microbiol Rev 59 1 1 30 7708009 1:CAS:528:DyaK2MXkvVGmur8%3D
24. K Hallberg E Gonzalez-Toril B Johnson 2010 Acidithiobacillus ferrivorans sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments Extremophiles 14 1 9 19 19787416 10.1007/s00792-009-0282-y 1:CAS:528:DC%2BC3cXjtlCitA%3D%3D
25. 2+ separately J Biochem Mol Biol 38 3 307 313 15943906 10.5483/BMBRep.2005.38.3.307 1:CAS:528:DC%2BD2MXlt1ygtr4%3D (Pubitemid 43034371)
26. W Jeamton S Mungpakdee M Sirijuntarut P Prommeenate S Cheevadhanarak M Tanticharoen A Hongsthong 2008 A combined stress response analysis of Spirulina platensis in terms of global differentially expressed proteins, and mRNA levels and stability of fatty acid biosynthesis genes FEMS Microbiol Lett 281 2 121 131 10.1111/j.1574-6968.2008.01100.x 1:CAS:528:DC%2BD1cXkslynurg%3D (Pubitemid 351422946)
27. CA Jerez M Seeger AM Amaro 1992 Phosphate starvation affects the synthesis of outer membrane proteins in Thiobacillus ferrooxidans FEMS Microbiol Lett 98 29 34 10.1111/j.1574-6968.1992.tb05485.x 1:CAS:528:DyaK3sXhvFSitQ%3D%3D
28. GI Karavaiko TP Turova TF Kondrat'eva AM Lysenko TV Kolganova SN Ageeva LN Muntyan TA Pivovarova 2003 Phylogenetic heterogeneity of the species Acidithiobacillus ferrooxidans Int J Syst Evol Microbiol 53 113 119 12656161 10.1099/ijs.0.02319-0 1:CAS:528:DC%2BD3sXitVSnt7g%3D (Pubitemid 36285229)
29. G Kramer A Rutkowska RD Wegrzyn H Patzelt TA Kurz F Merz T Rauch S Vorderwülbecke E Deuerling B Bukau 2004 Functional dissection of Escherichia coli Trigger Factor: Unraveling the function of individual domains J Bacteriol 186 12 3777 3784 15175291 10.1128/JB.186.12.3777-3784.2004 1:CAS:528:DC%2BD2cXkvFOrsrg%3D (Pubitemid 38746053)
30. C Krembs H Eicken K Junge JW Deming 2002 High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms Deep-Sea Research Part I: Oceanographic Research Papers 49 12 2163 2181 10.1016/S0967-0637(02)00122-X 1:CAS:528:DC%2BD3sXmsFeitg%3D%3D (Pubitemid 36178194)
31. F Kthiri H-T Le J Tagourti R Kern A Malki T Caldas J Abdallah A Landoulsi G Richarme 2008 The thioredoxin homolog YbbN functions as a chaperone rather than as an oxidoreductase Biochem Biophys Res Commun 374 4 668 672 18657513 10.1016/j.bbrc.2008.07.080 1:CAS:528:DC%2BD1cXhtValsr%2FL
32. D Kupka OI Rzhepishevska M Dopson EB Lindstrom OV Karnachuck OH Tuovinen 2007 Bacterial oxidation of ferrous iron at low temperatures Biotechnol Bioeng 97 6 1470 1478 17304566 10.1002/bit.21371 1:CAS:528:DC%2BD2sXotleqsLg%3D (Pubitemid 47204025)
33. K Kvint L Nachin A Diez T Nyström 2007 The bacterial universal stress protein: function and regulation Curr Opin Microbiol 6 2 140 145 10.1016/S1369-5274(03)00025-0
34. LG Leduc JT Trevors GD Ferroni 1993 Thermal characterization of different isolates of Thiobacillus ferrooxidans FEMS Microbiol Lett 108 189 194 10.1111/j.1574-6968.1993.tb06097.x 1:CAS:528:DyaK3sXisFWit7g%3D
35. BA Meth KE Nelson JW Deming B Momen E Melamud X Zhang 2005 The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses Proc Natl Acad Sci USA 102 31 10913 10918 10.1073/pnas.0504766102 (Pubitemid 41105967)
36. NCS Mykytczuk JT Trevors LG Leduc GD Ferroni 2007 Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress Prog Biophys MolBiol 95 60 82 10.1016/j.pbiomolbio.2007.05. 001 1:CAS:528:DC%2BD2sXhtFeitbbK (Pubitemid 47520624)
37. NCS Mykytczuk JT Trevors SM Twine GD Ferroni LG Leduc 2010 Membrane fluidity and fatty acid comparisons in psychrotrophic and mesophilic strains of Acidithiobacillus ferrooxidans under cold growth temperatures Arch Microbiol 192 12 1005 1018 20852847 10.1007/s00203-010-0629-x 1:CAS:528:DC%2BC3cXhsVegurvL
38. MTM Novo AC da Silva R Moreto PCP Cabral A Costacurta O Garcia Jr LMM Ottoboni 2000 Thiobacillus ferrooxidans response to copper and other heavy metals: growth, protein synthesis and protein phosphorylation Antonie van Leeuwenhoek 77 187 195 10768478 10.1023/A:1002462701671 1:STN:280: DC%2BD3c3ivV2ltw%3D%3D (Pubitemid 30160419)
39. MTM Novo O da Silva Garcia LMM Ottoboni Jr 2003 Protein profile of Acidithiobacillus ferrooxidans strains exhibiting different levels of tolerance to metal sulfates Curr Microbiol 47 492 496 14756533 10.1007/s00284-003-4096-3 1:CAS:528:DC%2BD3sXps1egsr0%3D (Pubitemid 37443148)
40. Piette F, D'Amico S, Mazzucchelli G, Danchin A, Leprince P, Feller G (2011) Life in the cold: a proteomic study of cold-repressed proteins in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Appl Environ Microbiol. doi: 10.1128/AEM.02757-10
41. Quatrini R, Valdes J, Jedlicki E, Holmes DS (2007) The use of Bioinformatics and genome biology to advance our understanding of bioleaching microorganisms. In: Donati ER, Sand W (eds) Microbial processing of metal sulfides. Springer, New York, NY
42. Raimann E, Schmid B, Stephan R, Tasara T (2009) The alternative sigma factor sigma(L) of L. monocytogenes promotes growth under diverse environmental stresses. Foodborne Pathog Dis 6(5):583-591
43. Ramagli LS (1999) Quantifying protein in 2-D PAGE solubilization buffers. In: Link AJ (ed) Methods in molecular biology, Clifton, NJ, pp 99-103
44. F Rodríguez-Quiñones M Maguire EJ Wallington PS Gould V Yerko JA Downie PA Lund 2005 Two of the three groEL homologues in Rhizobium leguminosarum are dispensable for normal growth Arch Microbiol 183 253 265 15830189 10.1007/s00203-005-0768-7 (Pubitemid 40768015)
45. JG Sklar T Wu D Kahne TJ Silhavy 2007 Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli Genes Dev 21 19 2473 2484 17908933 10.1101/gad.1581007 1:CAS:528:DC%2BD2sXhtFKrtL3I (Pubitemid 47529375)
46. St Denis LM (2008) Rapid identification of AMD bacteria through 16S rRNA gene sequencing MSc thesis, Laurentian University, Sudbury, Canada
47. HA Thieringer PA Jones M Inouye 1998 Cold shock and adaptation BioEssays 20 49 57 9504047 10.1002/(SICI)1521-1878(199801)20:1<49::AID-BIES8>3.0. CO;2-N 1:STN:280:DyaK1c7msVOqug%3D%3D (Pubitemid 28111331)
48. L Ting TJ Williams MJ Cowley FM Lauro M Guilhaus MJ Raftery R Cavicchioli 2010 Cold adaptation in the marine bacterium, Sphingopyxis alaskensis, assessed using quantitative proteomics Environ Microbiol 12 10 2658 2676 20482592 1:CAS:528:DC%2BC3cXhsVansbvP
49. A Tormo M Almiron R Kolter 1990 surA, an Escherichia coli gene essential for survival in stationary phase J Bacteriol 172 4339 4347 2165476 1:CAS:528:DyaK3cXkvFahsb4%3D (Pubitemid 20236723)
50. A Tosco L Birolo S Madonna G Lolli G Sannia G Marino 2003 GroEL from the psychrophilic bacterium Pseudoalteromonas haloplanktis TAC 125: molecular characterization and gene cloning Extremophiles 7 1 17 28 12579376 1:CAS:528:DC%2BD3sXhtVKktbw%3D (Pubitemid 40856323)
51. 2-fixation and iron oxidation as measures of growth Arch Microbiol 88 285 298 1:CAS:528:DyaE3sXmvFWltA%3D%3D
52. SM Twine NCS Mykytczuk M Petit T-L Tremblay JW Conlan JF Kelly 2005 Francisella tularensis proteome: low levels of ASB-14 facilitate the visualization of membrane proteins in total protein extracts J Proteome Res 4 5 1848 1854 16212441 10.1021/pr050102u 1:CAS:528:DC%2BD2MXntVygsLs%3D (Pubitemid 41464814)
53. SM Twine NCS Mykytczuk MD Petit H Shen A Sjöstedt JW Conlan JF Kelly 2006 In vivo proteomic analysis of the intracellular bacterial pathogen, Francisella tularensis, isolated from mouse spleen Biochem Biophys Res Commun 345 4 1621 1633 16730660 10.1016/j.bbrc.2006.05.070 1:CAS:528: DC%2BD28Xltl2gtr0%3D (Pubitemid 43817916)
54. SM Twine CJ Paul E Vinogradov DJ McNally J-R Brisson JA Mullen DR McMullin HC Jarrell JW Austin JF Kelly SM Logan 2008 Flagellar glycosylation in Clostridium botulinum FEBS J 275 17 4428 4444 18671733 10.1111/j.1742-4658.2008. 06589.x 1:CAS:528:DC%2BD1cXhtFCqtrrE
55. Valdés J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake II R, Eisen JA, Holmes DS (2008) Acidithiobacillus ferrooxidans metabolism: From genome sequence to industrial applications. BMC Genomics 9, art no. 597. doi: 10.1186/1471-2164-9-597
56. L Valenzuela A Chi S Beard A Orell N Guiliani J Shabanowitz DF Hunt CA Jarez 2006 Genomics, metagenomics and proteomics in biomining microorganisms Biotechnol Adv 24 197 211 16288845 10.1016/j.biotechadv.2005.09.004 1:CAS:528:DC%2BD28XhtVGjs78%3D (Pubitemid 43173509)
57. Wang Y, Delettre J, Guillot A, Corrieu G, Béal C (2005) Influence of cooling temperature and duration on cold adaptation of Lactobacillus acidophilus RD758. Cryobiology 50(3):294-307
58. F Wiegeshoff CL Beckering M Debarbouille MA Marahiel 2006 Sigma L is important for cold shock adaptation of Bacillus subtilis J Bacteriol 188 8 3130 3133 16585774 10.1128/JB.188.8.3130-3133.2006 1:CAS:528:DC%2BD28Xjslejtbg%3D
59. K Yamanaka 1999 Cold shock response in Escherichia coli J Mol Microbiol and Biotechnol 1 2 193 202 1:CAS:528:DyaK1MXnvF2htr8%3D (Pubitemid 129491941)
60. A Yarzábal C Appia-Ayme J Ratouchniak V Bonnefoy 2004 Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin Microbiology 150 2113 2123 15256554 10.1099/mic.0.26966-0 (Pubitemid 39117625)
61. K Yoshimune A Galkin L Kulakova T Yoshimura N Esaki 2005 Cold-active DnaK of an Antarctic psychrotroph Shewanella sp Ac10 supporting the growth of dnaK-null mutant of Escherichia coli at cold temperatures Extremophiles 9 2 145 150 15599780 10.1007/s00792-004-0429-9 1:CAS:528:DC%2BD2MXjtlKqtb8%3D (Pubitemid 40660354)