Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: A genome and transcriptome approach

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Rodrigues, Debora F ^a   Ivanova, Natalia ^b   He, Zhili ^c   Huebner, Marianne ^a   Zhou, Jizhong ^c   Tiedje, James M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b DOE JOINT GENOME INSTITUTE   (United States)

^c UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOHYDRATE; CYTOSINE; GUANINE; TRANSCRIPTOME; NUCLEOTIDE;

AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATION; CARBOHYDRATE METABOLISM; DNA CONTENT; DNA MICROARRAY; EXIGUOBACTERIUM SIBIRICUM; GENE EXPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; GRAM POSITIVE BACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PERMAFROST; PLASMID; RNA ISOLATION; STRESS; TEMPERATURE ACCLIMATIZATION; TRANSMISSION ELECTRON MICROSCOPY; ACCLIMATIZATION; COLD; DNA REPLICATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; GRAM POSITIVE ASPOROGENOUS ROD-SHAPED BACTERIA; METABOLISM; PHYSIOLOGY; RUSSIAN FEDERATION; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); EXIGUOBACTERIUM;

ACCLIMATIZATION; AMINO ACIDS; CARBOHYDRATE METABOLISM; COLD TEMPERATURE; DNA REPLICATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENOME, BACTERIAL; GRAM-POSITIVE ASPOROGENOUS RODS; MICROSCOPY, ELECTRON, TRANSMISSION; NUCLEOTIDES; SIBERIA; TRANSCRIPTION, GENETIC;

EID: 58149510474     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-547     Document Type: Article

References (68)

1. Kawahara H Koda N Oshio M Obata H A cold acclimation protein with refolding activity on frozen denatured enzymes Biosci Biotechnol Biochem 2000, 64(12):2668-2674. 10.1271/bbb.64.2668 11210132
2. Russell NJ Cold adaptation of microorganisms Philos Trans R Soc Lond B Biol Sci 1990, 326(1237): 595-608. discussion 608-511. 10.1098/ rstb.1990.0034 1969649
3. Vishnivetskaya T Kathariou S McGrath J Gilichinsky D Tiedje JM Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments Extremophiles 2000, 4(3):165-173. 10.1007/ s007920070031 10879561
4. Morita RY Psychrophilic bacteria Bacteriol Rev 1975, 39(2):144-167. 413900 1095004
5. Gounot AM Bacterial life at low temperature: Physiological aspects and biotechnological implications J Appl Bacteriol 1991, 71(5):386-397. 1761432
6. Bierne H Cossart P Listeria monocytogenes surface proteins: From genome predictions to function Microbiol Mol Biol Rev 2007, 71(2):377-397. 1899877 17554049 10.1128/MMBR.00039-06
7. Methe BA Nelson KE Deming JW Momen B Melamud E Zhang X Moult J Madupu R Nelson WC Dodson RJ et al. The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses Proc Natl Acad Sci USA 2005, 102(31):10913-10918. 1180510 16043709 10.1073/pnas.0504766102
8. Hou S Saw JH Lee KS Freitas TA Belisle C Kawarabayasi Y Donachie SP Pikina A Galperin MY Koonin EV et al. Genome sequence of the deep-sea gamma-proteobacterium Idiomarina loihiensis reveals amino acid fermentation as a source of carbon and energy Proc Natl Acad Sci USA 2004, 101(52):18036-18041. 539801 15596722 10.1073/pnas.0407638102
9. Medigue C Krin E Pascal G Barbe V Bernsel A Bertin PN Cheung F Cruveiller S D'Amico S Duilio A et al. Coping with cold: The genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125 Genome Res 2005, 15(10):1325-1335. 1240074 16169927 10.1101/ gr.4126905
10. Riley M Staley JT Danchin A Wang T Brettin TS Hauser LJ Land ML Thompson LS Genomics of an extreme psychrophile, Psychromonas ingrahamii BMC Genomics 2008, 9(1):210. 2405808 18460197
11. Thieringer HA Jones PG Inouye M Cold shock and adaptation Bioessays 1998, 20(1):49-57. 10.1002/ (SICI)1521-1878(199801)20:1<49::AID-BIES8>3.0.CO;2-N 9504047
12. Phadtare S Alsina J Inouye M Cold-shock response and cold-shock proteins Curr Opin Microbiol 1999, 2(2):175-180. 10.1016/S1369-5274(99)80031-9 10322168
13. Gao H Yang ZK Wu L Thompson DK Zhou J Global transcriptome analysis of the cold shock response of Shewanella oneidensis MR-1 and mutational analysis of its classical cold shock proteins J Bacteriol 2006, 188(12):4560-4569. 1482949 16740962 10.1128/JB.01908-05
14. Guillou C Guespin-Michel JF Evidence for two domains of growth temperature for the psychrotrophic bacterium Pseudomonas fluorescens MF0 Appl Environ Microbiol 1996, 62(9):3319-3324. 168127 8795221
15. Herendeen SL VanBogelen RA Neidhardt FC Levels of major proteins of Escherichia coli during growth at different temperatures J Bacteriol 1979, 139(1):185-194. 216844 156716
16. Rodrigues DF Goris J Vishnivetskaya T Gilichinsky D Thomashow MF Tiedje JM Characterization of Exiguobacterium isolates from the Siberian permafrost. Description of Exiguobacterium sibiricum sp. nov Extremophiles 2006, 10(4):285-294. 10.1007/s00792-005-0497-5 16489412
17. Rodrigues DF Tiedje JM Multi-locus real-time PCR for quantitation of bacteria in the environment reveals Exiguobacterium to be prevalent in permafrost FEMS Microbiol Ecol 2007, 59(2):489-499. 17156079
18. Chaturvedi P Shivaji S Exiguobacterium indicum sp. nov., a psychrophilic bacterium from the Hamta glacier of the Himalayan mountain ranges of India Int J Syst Evol Microbiol 2006, 56(Pt 12):2765-2770. 10.1099/ ijs.0.64508-0 17158975
19. Fruhling A Schumann P Hippe H Straubler B Stackebrandt E Exiguobacterium undae sp. nov. and Exiguobacterium antarcticum sp. nov Int J Syst Evol Microbiol 2002, 52(Pt 4):1171-1176. 10.1099/ijs.0.02185-0 12148624
20. Vishnivetskaya TA Petrova MA Urbance J Ponder M Moyer CL Gilichinsky DA Tiedje JM Bacterial community in ancient siberian permafrost as characterized by culture and culture-independent methods Astrobiology 2006, 6(3):400-414. 10.1089/ast.2006.6.400 16805696
21. Ponder MA Gilmour SJ Bergholz PW Mindock CA Hollingsworth R Thomashow MF Tiedje JM Characterization of potential stress responses in ancient Siberian permafrost psychroactive bacteria FEMS Microbiol Ecol 2005, 53(1):103-115. 10.1016/j.femsec.2004.12.003 16329933
22. Karlin S Theriot J Mrazek J Comparative analysis of gene expression among low G+C gram-positive genomes Proc Natl Acad Sci USA 2004, 101(16):6182-6187. 395943 15069198 10.1073/pnas.0401504101
23. Wu J Woodard RW New insights into the evolutionary links relating to the 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase subfamilies J Biol Chem 2006, 281(7):4042-4048. 10.1074/jbc.M512223200 16339761
24. Zhao G Xia T Aldrich H Jensen RA Cyclohexadienyl dehydratase from Pseudomonas aeruginosa is a periplasmic protein J Gen Microbiol 1993, 139(4):807-813. 8515238
25. Margesin R Schinner F Efficiency of Indigenous and Inoculated Cold-Adapted Soil Microorganisms for Biodegradation of Diesel Oil in Alpine Soils Appl Environ Microbiol 1997, 63(7):2660-2664. 1389197 16535642
26. Gerday C Aittaleb M Arpigny JL Baise E Chessa JP Garsoux G Petrescu I Feller G Psychrophilic enzymes: A thermodynamic challenge Biochim Biophys Acta 1997, 1342(2):119-131. 9392521
27. Gianese G Argos P Pascarella S Structural adaptation of enzymes to low temperatures Protein Eng 2001, 14(3):141-148. 10.1093/protein/14.3.141 11342709
28. Carpenter JH New measurements of oxygen solubility in pure and natural water Limnol Oceanog 1966, 11(2):246-277.
29. Wyk PV Scarpa J Water Quality Requirements and Management Farming marine shrimp in recirculating freshwater systmes Florida department of agriculture and consumer services Wyk PV, Davis-Hodgkins M, Laramore R, Main LK, Mountain J, Scarpa J 1999:141-162.
30. White D The physiology and biochemistry of Prokaryotes NY: Oxford University Press 2 2000
31. Brigulla M Hoffmann T Krisp A Volker A Bremer E Volker U Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation J Bacteriol 2003, 185(15):4305-4314. 165770 12867438 10.1128/JB.185.15.4305-4314.2003
32. Bayles DO Wilkinson BJ Osmoprotectants and cryoprotectants for Listeria monocytogenes Lett Appl Microbiol 2000, 30(1):23-27. 10.1046/ j.1472-765x.2000.00646.x 10728555
33. Ko R Smith LT Smith GM Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes J Bacteriol 1994, 176(2):426-431. 205066 8288538
34. Dinnbier U Limpinsel E Schmid R Bakker EP Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations Arch Microbiol 1988, 150(4):348-357. 10.1007/BF00408306 3060036
35. Mazur P The role of intracellular freezing in the death of cells cooled at supraoptimal rates Cryobiology 1977, 14(3):251-272. 10.1016/ 0011-2240(77)90175-4 330113
36. Mayer RR Cherry JH Rhodes D Effects of Heat Shock on Amino Acid Metabolism of Cowpea Cells Plant Physiol 1990, 94(2):796-810. 1077301 16667781 10.1104/pp.94.2.796
37. Murata N Wada H Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria Biochem J 1995, 308(Pt 1):1-8. 1136835 7755550
38. Ray MK Kumar GS Janiyani K Kannan K Jagtap P Basu MK Shivaji S Adaptation to low temperature and regulation of gene expression in antarctic psychrotrophic bacteria J Biosci 1998, 23(4):423-435. 10.1007/ BF02936136
39. Russell NJ Mechanism for thermal adaptation in bacteria: Blueprint for survival Trends Biochem Sci 1984, 9:108-112. 10.1016/0968-0004(84)90106-3
40. Golovlev EL [Bacterial cold shock response at the level of DNA transcription, translation and chromosome dynamics] Mikrobiologiia 2003, 72(1):5-13. 12698785
41. Rodrigues DF Tiedje JM Coping With Our Cold Planet Appl Environ Microbiol 2008, 74(6):1677-1686. 2268296 18203855 10.1128/AEM.02000-07
42. Wada H Murata N Synechocystis PCC6803 mutants defective in desaturation of fatty acids Plant Cell Physiol 1989, 30(7):971-978.
43. Carty SM Sreekumar KR Raetz CR Effect of cold shock on lipid A biosynthesis in Escherichia coli. Induction At 12 degrees C of an acyltransferase specific for palmitoleoyl-acyl carrier protein J Biol Chem 1999, 274(14):9677-9685. 10.1074/jbc.274.14.9677 10092655
44. Klein W Weber MH Marahiel MA Cold shock response of Bacillus subtilis: isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures J Bacteriol 1999, 181(17):5341-5349. 94040 10464205
45. Lopez-Garcia P Forterre P Control of DNA topology during thermal stress in hyperthermophilic archaea: DNA topoisomerase levels, activities and induced thermotolerance during heat and cold shock in Sulfolobus Mol Microbiol 1999, 33(4):766-777. 10.1046/j.1365-2958.1999.01524.x 10447886
46. Gualerzi CO Giuliodori AM Pon CL Transcriptional and post-transcriptional control of cold-shock genes J Mol Biol 2003, 331(3):527-539. 10.1016/S0022-2836(03)00732-0 12899826
47. Scherer S Neuhaus K Life at low temperature The Prokaryotes: An evolving electronic resource for the microbiological community New York: Springer-Verlag Dworkin MEA 2002:3.
48. Weber MH Marahiel MA Bacterial cold shock responses Sci Prog 2003, 86(Pt 1-2):9-75. 10.3184/003685003783238707 12838604
49. Helmann JD Wu MF Kobel PA Gamo FJ Wilson M Morshedi MM Navre M Paddon C Global transcriptional response of Bacillus subtilis to heat shock J Bacteriol 2001, 183(24):7318-7328. 95581 11717291 10.1128/ JB.183.24.7318-7328.2001
50. Pysz MA Ward DE Shockley KR Montero CI Conners SB Johnson MR Kelly RM Transcriptional analysis of dynamic heat-shock response by the hyperthermophilic bacterium Thermotoga maritima Extremophiles 2004, 8(3):209-217. 10.1007/s00792-004-0379-2 14991425
51. Friedman DI Olson ER Georgopoulos C Tilly K Herskowitz I Banuett F Interactions of bacteriophage and host macromolecules in the growth of bacteriophage lambda Microbiol Rev 1984, 48(4):299-325. 373221 6240590
52. Ramos JL Gallegos MT Marques S Ramos-Gonzalez MI Espinosa-Urgel M Segura A Responses of Gram-negative bacteria to certain environmental stressors Curr Opin Microbiol 2001, 4(2):166-171. 10.1016/S1369-5274(00)00183-1 11282472
53. Donovan WP Kushner SR Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12 Proc Natl Acad Sci USA 1986, 83(1):120-124. 322803 2417233 10.1073/ pnas.83.1.120
54. De Angelis M Di Cagno R Huet C Crecchio C Fox PF Gobbetti M Heat shock response in Lactobacillus plantarum Appl Environ Microbiol 2004, 70(3):1336-1346. 368309 15006751 10.1128/AEM.70.3.1336-1346.2004
55. Shukla HD 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. 1475562 16623945 10.1186/1477-5956-4-6
56. Scott JM Ju J Mitchell T Haldenwang WG The Bacillus subtilis GTP binding protein obg and regulators of the sigma(B) stress response transcription factor cofractionate with ribosomes J Bacteriol 2000, 182(10):2771-2777. 101985 10781545 10.1128/JB.182.10.2771-2777.2000
57. Schumann W The Bacillus subtilis heat shock stimulon Cell Stress Chaperones 2003, 8(3):207-217. 514873 14984053 10.1379/ 1466-1268(2003)008<0207:TBSHSS>2.0.CO;2
58. Derre I Rapoport G Msadek T CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria Mol Microbiol 1999, 31(1):117-131. 10.1046/ j.1365-2958.1999.01152.x 9987115
59. Yura T Nakahigashi K Regulation of the heat-shock response Current Opinion in Microbiology 1999, 2(2):153-158. 10.1016/ S1369-5274(99)80027-7 10322172
60. Qiu Y Kathariou S Lubman DM Proteomic analysis of cold adaptation in a Siberian permafrost bacterium-Exiguobacterium sibiricum 255-15 by two-dimensional liquid separation coupled with mass spectrometry Proteomics 2006, 6(19):5221-5233. 10.1002/pmic.200600071 16955517
61. Li X He Z Zhou J Selection of optimal oligonucleotide probes for microarrays using multiple criteria, global alignment and parameter estimation Nucleic Acids Res 2005, 33(19):6114-6123. 1266071 16246912 10.1093/nar/gki914
62. He Z Wu L Li X Fields MW Zhou J Empirical establishment of oligonucleotide probe design criteria Appl Environ Microbiol 2005, 71(7):3753-3760. 1169010 16000786 10.1128/AEM.71.7.3753-3760.2005
63. Rainer J Sanchez-Cabo F Stocker G Sturn A Trajanoski Z CARMAweb: comprehensive R- and bioconductor-based web service for microarray data analysis Nucleic Acids Res 2006, 34;Web Server W498-503. 1538903 16845058 10.1093/nar/gkl038
64. Benjamini Y Hochberg Y Controlling the false discovery rate: A practical and powerful approach to multiple testing J R Stat Soc Ser 1995, 57:289-300.
65. Westfall PH Young S Resampling-Based Multiple Testing: Examples and Methods for P-value adjustment NY: Wiley 1993.
66. Rice P Longden I Bleasby A EMBOSS: The European Molecular Biology Open Software Suite Trends Genet 2000, 16(6):276-277. 10.1016/ S0168-9525(00)02024-2 10827456
67. Frishman D Argos P Knowledge-based protein secondary structure assignment Proteins 1995, 23(4):566-579. 10.1002/prot.340230412 8749853
68. Néron B Ménager H Maufrais C Joly N Tufféry P Maupetit J Letondal C Mobyle: A new full web bioinformatics framework Bio Open Source Conference (BOSC): Toronto 2008.