The survival mechanisms of thermophiles at high temperatures: An angle of omics

Physiology

Volumn 30, Issue 2, 2015, Pages 97-106

  Wang, Quanhui ^a,b   Cen, Zhen ^a   Zhao, Jingjing ^a  

^a Chinese Academy of Sciences   (China)

^b BGI SHENZHEN   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ADAPTATION; BACTERIUM; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; HEAT; METABOLISM; METABOLOMICS; MICROBIAL VIABILITY; MOLECULAR EVOLUTION; PROCEDURES; PROTEIN STABILITY; PROTEOMICS;

ADAPTATION, PHYSIOLOGICAL; BACTERIA; BACTERIAL PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; GENOMICS; HOT TEMPERATURE; METABOLOMICS; MICROBIAL VIABILITY; PROTEIN STABILITY; PROTEOMICS;

EID: 84924039501     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00066.2013     Document Type: Review

References (90)

1. Aravind L, Tatusov RL, Wolf YI, Walker DR, Koonin EV. Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet 14: 442-444, 1998.
2. Arnorsdottir J, Sigtryggsdottir AR, Thorbjarnardottir SH, Kristjansson MM. Effect of proline substitutions on stability and kinetic properties of a cold adapted subtilase. J Biochem 145: 325-329, 2009.
3. Atomi H, Matsumi R, Imanaka T. Reverse gyrase is not a prerequisite for hyperthermophilic life. J Bacteriol 186: 4829-4833, 2004.
4. Averhoff B, Muller V. Exploring research frontiers in microbiology: recent advances in halophilic and thermophilic extremophiles. Res Microbiol 161: 506-514, 2010.
5. Bao Q, Tian Y, Li W, Xu Z, Xuan Z, Hu S, Dong W, Yang J, Chen Y, Xue Y, Xu Y, Lai X, Huang L, Dong X, Ma Y, Ling L, Tan H, Chen R, Wang J, Yu J, Yang H. A complete sequence of the T. tengcongensis genome. Genome Res 12: 689-700, 2002.
6. Barabote RD, Xie G, Leu DH, Normand P, Necsulea A, Daubin V, Medigue C, Adney WS, Xu XC, Lapidus A, Parales RE, Detter C, Pujic P, Bruce D, Lavire C, Challacombe JF, Brettin TS, Berry AM. Complete genome of the cellulolytic thermophile Acidothermus cellulolyticus 11B provides insights into its ecophysiological and evolutionary adaptations. Genome Res 19: 1033-1043, 2009.
7. Basak S, Banerjee T, Gupta SK, Ghosh TC. Investigation on the causes of codon and amino acid usages variation between thermophilic Aquifex aeolicus and mesophilic Bacillus subtilis. J Biomol Struct Dyn 22: 205-214, 2004.
8. Basak S, Mukhopadhyay P, Gupta SK, Ghosh TC. Genomic adaptation of prokaryotic organisms at high temperature. Bioinformation 4: 352-356, 2010.
9. Beeby M, O'Connor BD, Ryttersgaard C, Boutz DR, Perry LJ, Yeates TO. The genomics of disulfide bonding and protein stabilization in thermophiles. PLoS Biol 3: e309, 2005.
10. Bezsudnova EY, Boyko KM, Polyakov KM, Dorovatovskiy PV, Stekhanova TN, Gumerov VM, Ravin NV, Skryabin KG, Kovalchuk MV, Popov VO. Structural insight into the molecular basis of polyextremophilicity of short-chain alcohol dehydrogenase from the hyperthermophilic archaeon Thermococcus sibiricus. Biochimie 94: 2628-2638, 2012.
11. Blaby IK, Lyons BJ, Wroclawska-Hughes E, Phillips GC, Pyle TP, Chamberlin SG, Benner SA, Lyons TJ, Crecy-Lagard V, Crecy E. Experimental evolution of a facultative thermophile from a mesophilic ancestor. Appl Environ Microbiol 78: 144- 155, 2012.
12. Blumer-Schuette SE, Ozdemir I, Mistry D, Lucas S, Lapidus A, Cheng JF, Goodwin LA, Pitluck S, Land ML, Hauser LJ, Woyke T, Mikhailova N, Pati A, Kyrpides NC, Ivanova N, Detter JC, Walston-Davenport K, Han S, Adams MW, Kelly RM. Complete genome sequences for the anaerobic, extremely thermophilic plant biomass-degrading bacteria Caldicellulosiruptor hydrothermalis, Caldicellulosiruptor kristjanssonii, Caldicellulosiruptor kronotskyensis, Caldicellulosiruptor owensensis, and Caldicellulosiruptor lactoaceticus. J Bacteriol 193: 1483-1484, 2011.
13. Boto L. Horizontal gene transfer in the acquisition of novel traits by metazoans. Proc Biol Sci 281: 20132450, 2014.
14. Boutz DR, Cascio D, Whitelegge J, Perry LJ, Yeates TO. Discovery of a thermophilic protein complex stabilized by topologically interlinked chains. J Mol Biol 368: 1332-1344, 2007.
15. Browning DF, Busby SJ. The regulation of bacterial transcription initiation. Nat Rev Microbiol 2: 57-65, 2004.
16. Burra PV, Kalmar L, Tompa P. Reduction in structural disorder and functional complexity in the thermal adaptation of prokaryotes. PLos One 5: e12069, 2010.
17. Cacciapuoti G, Moretti MA, Forte S, Brio A, Camardella L, Zappia V, Porcelli M. Methylthioadenosine phosphorylase from the archaeon Pyrococcus furiosus. Mechanism of the reaction and assignment of disulfide bonds. Eur J Biochem 271: 4834-4844, 2004.
18. Chen J, Stites WE. Replacement of staphylococcal nuclease hydrophobic core residues with those from thermophilic homologues indicates packing is improved in some thermostable proteins. J Mol Biol 344: 271-280, 2004.
19. Chen Z, Wang Q, Lin L, Tang Q, Edwards JL, Li S, Liu S. Comparative evaluation of two isobaric labeling tags, DiART and iTRAQ. Anal Chem 84: 2908-2915, 2012.
20. Chen Z, Wen B, Wang Q, Tong W, Guo J, Bai X, Zhao J, Sun Y, Tang Q, Lin Z, Lin L, Liu S. Quantitative proteomics reveals the temperature-dependent proteins encoded by a series of cluster genes in thermoanaerobacter tengcongensis. Mol Cell Proteomics 12: 2266-2277, 2013.
21. Chen Z, Wen B, Wang Q, Tong W, Guo J, Bai X, Zhao J, Sun Y, Tang Q, Lin Z, Lin L, Liu S. Quantitative proteomics reveals the temperature-dependent proteins encoded by a series of cluster genes in Thermoanaerobacter tengcongensis. Mol Cell Proteomics 12: 2266-2277, 2013.
22. Cooper CR, Daugherty AJ, Tachdjian S, Blum PH, Kelly RM. Role of vapBC toxin-antitoxin loci in the thermal stress response of Sulfolobus solfataricus. Biochem Soc Trans 37: 123-126, 2009.
23. Das S, Paul S, Bag SK, Dutta C. Analysis of Nanoarchaeum equitans genome and proteome composition: indications for hyperthermophilic and parasitic adaptation. BMC Genomics 7: 186, 2006.
24. Drake JW. Avoiding dangerous missense: thermophiles display especially low mutation rates. Plos Genet 5: e1000520, 2009.
25. Dutta A, Chaudhuri K. Analysis of tRNA composition and folding in psychrophilic, mesophilic and thermophilic genomes: indications for thermal adaptation. FEMS Microbiol Lett 305: 100-108, 2010.
26. Farhoud MH, Wessels HJ, Steenbakkers PJ, Mattijssen S, Wevers RA, van Engelen BG, Jetten MS, Smeitink JA, van den Heuvel LP, Keltjens JT. Protein complexes in the archaeon Methanothermobacter thermautotrophicus analyzed by blue native/SDS-PAGE and mass spectrometry. Mol Cell Proteomics 4: 1653-1663, 2005.
27. Farias ST, Bonato MC. Preferred amino acids and thermostability. Genet Mol Res 2: 383-393, 2003.
28. Feng S, Powell SM, Wilson R, Bowman JP. Extensive gene acquisition in the extremely psychrophilic bacterial species Psychroflexus torquis and the link to sea-ice ecosystem specialism. Genome Biol Evol 6: 133-148, 2014.
29. Forterre P, Bouthier De La Tour C, Philippe H, Duguet M. Reverse gyrase from hyperthermophiles: probable transfer of a thermoadaptation trait from archaea to bacteria. Trends Genet 16: 152-154, 2000.
30. Friedman R, Drake JW, Hughes AL. Genome-wide patterns of nucleotide substitution reveal stringent functional constraints on the protein sequences of thermophiles. Genetics 167: 1507-1512, 2004.
31. Gao H, Wang Y, Liu X, Yan T, Wu L, Alm E, Arkin A, Thompson DK, Zhou J. Global transcriptome analysis of the heat shock response of Shewanella oneidensis. J Bacteriol 186: 7796-7803, 2004.
32. Gu J, Hilser VJ. Sequence-based analysis of protein energy landscapes reveals nonuniform thermal adaptation within the proteome. Mol Biol Evol 26: 2217-2227, 2009.
33. Hakulinen N, Turunen O, Janis J, Leisola M, Rouvinen J. Three-dimensional structures of thermophilic beta-1,4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa. Comparison of twelve xylanases in relation to their thermal stability. Eur J Biochem 270: 1399-1412, 2003.
34. Heine M, Chandra SB. The linkage between reverse gyrase and hyperthermophiles: a review of their invariable association. J Microbiol 47: 229-234, 2009.
35. Heinemann J, Hamerly T, Maaty WS, Movahed N, Steffens JD, Reeves BD, Hilmer JK, Therien J, Grieco PA, Peters JW, Bothner B. Expanding the paradigm of thiol redox in the thermophilic root of life. Biochim Biophys Acta 1840: 80-85, 2013.
36. Hickey DA, Singer GA. Genomic and proteomic adaptations to growth at high temperature. Genome Biol 5: 117, 2004.
37. Jaenicke R. Stability and stabilization of globular proteins in solution. J Biotechnol 79: 193-203, 2000.
38. Jiang L, Lin M, Li X, Cui H, Xu X, Li S, Huang H. Genome sequence of Thermus thermophilus ATCC 33923, a thermostable trehalose-producing strain. Genome Announc 1: e00493-e00513, 2013.
39. Johnson MR, Conners SB, Montero CI, Chou CJ, Shockley KR, Kelly RM. The Thermotoga maritima phenotype is impacted by syntrophic interaction with Methanococcus jannaschii in hyperthermophilic coculture. Appl Environ Microbiol 72: 811-818, 2006.
40. Jones PG, Inouye M. RbfA, a 30S ribosomal binding factor, is a cold-shock protein whose absence triggers the cold-shock response. Mol Microbiol 21: 1207-1218, 1996.
41. Jorda J, Yeates TO. Widespread disulfide bonding in proteins from thermophilic archaea. Archaea 2011: 409156, 2011.
42. Kissling GE, Grogan DW, Drake JW. Confounders of mutation-rate estimators: selection and phenotypic lag in Thermus thermophilus. Mutat Res 749: 16-20, 2013.
43. Kreil DP, Ouzounis CA. Identification of thermophilic species by the amino acid compositions deduced from their genomes. Nucleic Acids Res 29: 1608-1615, 2001.
44. Li H, Ji X, Zhou Z, Wang Y, Zhang X. Thermus thermophilus proteins that are differentially expressed in response to growth temperature and their implication in thermoadaptation. J Proteome Res 9: 855-864, 2010.
45. Li X, Xing J, Li B, Yu F, Lan X, Liu J. Phylogenetic analysis reveals the coexistence of interfamily and interspecies horizontal gene transfer in Streptococcus thermophilus strains isolated from the same yoghurt. Mol Phylogenet Evol 69: 286- 292, 2013.
46. Lindsay JA. Staphylococcus aureus genomics and the impact of horizontal gene transfer. Int J Med Microbiol 304: 103-109, 2014.
47. Littlechild JA, Guy JE, Isupov MN. Hyperthermophilic dehydrogenase enzymes. Biochem Soc Trans 32: 255-258, 2004.
48. Liu L, Wang L, Zhang Z, Wang S, Chen H. Effect of codon message on xylanase thermal activity. J Biol Chem 287: 27183-27188, 2012.
49. Lobry JR, Necsulea A. Synonymous codon usage and its potential link with optimal growth temperature in prokaryotes. Gene 385: 128-136, 2006.
50. Loftie-Eaton W, Taylor M, Horne K, Tuffin MI, Burton SG, Cowan DA. Balancing redox cofactor generation and ATP synthesis: key microaerobic responses in thermophilic fermentations. Biotechnol Bioeng 110: 1057-1065, 2013.
51. Lynn DJ, Singer GA, Hickey DA. Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res 30: 4272-4277, 2002.
52. Mahale KN, Kempraj V, Dasgupta D. Does the growth temperature of a prokaryote influence the purine content of its mRNAs? Gene 497: 83-89, 2012.
53. Mallick P, Boutz DR, Eisenberg D, Yeates TO. Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc Natl Acad Sci USA 99: 9679-9684, 2002.
54. Meng B, Qian Z, Wei F, Wang W, Zhou C, Wang Z, Wang Q, Tong W, Ma Y, Xu N, Liu S. Proteomic analysis on the temperature-dependent complexes in Thermoanaerobacter tengcongensis. Proteomics 9: 3189-3200, 2009.
55. Mizobata T, Kagawa M, Murakoshi N, Kusaka E, Kameo K, Kawata Y, Nagai J. Overproduction of Thermus sp. YS 8-13 manganese catalase in Escherichia coli production of soluble apoenzyme and in vitro formation of active holoenzyme. Eur J Biochem 267: 4264-4271, 2000.
56. Muller JE, Litsanov B, Bortfeld-Miller M, Trachsel C, Grossmann J, Brautaset T, Vorholt JA. Proteomic analysis of the thermophilic methylotroph Bacillus methanolicus MGA3. Proteomics 14: 725-737, 2014.
57. Musto H, Naya H, Zavala A, Romero H, Alvarez- Valin F, Bernardi G. The correlation between genomic G+C and optimal growth temperature of prokaryotes is robust: a reply to Marashi and Ghalanbor. Biochem Biophys Res Commun 330: 357-360, 2005.
58. Musto H, Naya H, Zavala A, Romero H, Alvarez- Valin F, Bernardi G. Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochem Biophys Res Commun 347: 1-3, 2006.
59. Nakka M, Iyer RB, Bachas LG. Intersubunit disulfide interactions play a critical role in maintaining the thermostability of glucose-6-phosphate dehydrogenase from the hyperthermophilic bacterium Aquifex aeolicus. Protein J 25: 17-21, 2006.
60. Nelson KE, Clayton RA, Gill SR, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Nelson WC, Ketchum KA, McDonald L, Utterback TR, Malek JA, Linher KD, Garrett MM, Stewart AM, Cotton MD, Pratt MS, Phillips CA, Richardson D, Heidelberg J, Sutton GG, Fleischmann RD, Eisen JA, White O, Salzberg SL, Smith HO, Venter JC, Fraser CM. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399: 323-329, 1999.
61. Omelchenko MV, Wolf YI, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Daly MJ, Koonin EV, Makarova KS. Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: divergent routes of adaptation to thermophily and radiation resistance. BMC Evol Biol 5: 57, 2005.
62. Pang J, Allemann RK. Molecular dynamics simulation of thermal unfolding of Thermatoga maritima DHFR. Phys Chem Chem Phys 9: 711-718, 2007.
63. Paz A, Mester D, Baca I, Nevo E, Korol A. Adaptive role of increased frequency of polypurine tracts in mRNA sequences of thermophilic prokaryotes. Proc Natl Acad Sci USA 101: 2951- 2956, 2004.
64. Pedone E, Ren B, Ladenstein R, Rossi M, Bartolucci S. Functional properties of the protein disulfide oxidoreductase from the archaeon Pyrococcus furiosus: a member of a novel protein family related to protein disulfide-isomerase. Eur J Biochem 271: 3437-3448, 2004.
65. Perugino G, Valenti A, D'Amaro A, Rossi M, Ciaramella M. Reverse gyrase and genome stability in hyperthermophilic organisms. Biochem Soc Trans 37: 69-73, 2009.
66. 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 8: 209-217, 2004.
67. Qian Z, Zhao J, Bai X, Tong W, Chen Z, Wei H, Wang Q, Liu S. Thermal stability of glucokinases in Thermoanaerobacter tengcongensis. Bio Med Res Intl 2013: 646539, 2013.
68. Running WE, Reilly JP. Ribosomal proteins of Deinococcus radiodurans: their solvent accessibility and reactivity. J Proteome Res 8: 1228- 1246, 2009.
69. Sabath N, Ferrada E, Barve A, Wagner A. Growth temperature and genome size in bacteria are negatively correlated, suggesting genomic streamlining during thermal adaptation. Genome Biol Evol 5: 966-977, 2013.
70. Saunders NF, Thomas T, Curmi PM, Mattick JS, Kuczek E, Slade R, Davis J, Franzmann PD, Boone D, Rusterholtz K, Feldman R, Gates C, Bench S, Sowers K, Kadner K, Aerts A, Dehal P, Detter C, Glavina T, Lucas S, Richardson P, Larimer F, Hauser L, Land M, Cavicchioli R. Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13: 1580-1588, 2003.
71. Shcherbakov D, Dontsova M, Tribus M, Garber M, Piendl W. Stability of the 'L12 stalk' in ribosomes from mesophilic and (hyper)thermophilic Archaea and Bacteria. Nucleic Acids Res 34: 5800-5814, 2006.
72. Shih TW, Pan TM. Stress responses of thermophilic Geobacillus sp. NTU 03 caused by heat and heat-induced stress. Microbiol Res 166: 346-359, 2011.
73. Shockley KR, Ward DE, Chhabra SR, Conners SB, Montero CI, Kelly RM. Heat shock response by the hyperthermophilic archaeon Pyrococcus furiosus. Appl Environ Microbiol 69: 2365-2371, 2003.
74. Singer GA, Hickey DA. Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene 317: 39-47, 2003.
75. Takami H, Takaki Y, Chee GJ, Nishi S, Shimamura S, Suzuki H, Matsui S, Uchiyama I. Thermoadaptation trait revealed by the genome sequence of thermophilic Geobacillus kaustophilus. Nucleic Acids Res 32: 6292-6303, 2004.
76. Teh BS, Abdul Rahman AY, Saito JA, Hou S, Alam M. Complete genome sequence of the thermophilic bacterium Thermus sp. strain CCB_ US3_UF1. J Bacteriol 194: 1240, 2012.
77. Tekaia F, Yeramian E, Dujon B. Amino acid composition of genomes, lifestyles of organisms, and evolutionary trends: a global picture with correspondence analysis. Gene 297: 51-60, 2002.
78. Trauger SA, Kalisak E, Kalisiak J, Morita H, Weinberg MV, Menon AL, Poole FL, 2nd Adams MW, Siuzdak G. Correlating the transcriptome, proteome, and metabolome in the environmental adaptation of a hyperthermophile. J Proteome Res 7: 1027-1035, 2008.
79. van Noort V, Bradatsch B, Arumugam M, Amlacher S, Bange G, Creevey C, Falk S, Mende DR, Sinning I, Hurt E, Bork P. Consistent mutational paths predict eukaryotic thermostability. BMC Evol Biol 13: 7, 2013.
80. van Wolferen M, Ajon M, Driessen AJ, Albers SV. How hyperthermophiles adapt to change their lives: DNA exchange in extreme conditions. Extremophiles 17: 545-563, 2013.
81. Vettone A, Perugino G, Rossi M, Valenti A, Ciaramella M. Genome stability: recent insights in the topoisomerase reverse gyrase and thermophilic DNA alkyltransferase. Extremophiles 18: 895- 904, 2014.
82. Wang HC, Susko E, Roger AJ. On the correlation between genomic G+C content and optimal growth temperature in prokaryotes: data quality and confounding factors. Biochem Biophys Res Commun 342: 681-684, 2006.
83. Wang HC, Xia X, Hickey D. Thermal adaptation of the small subunit ribosomal RNA gene: a comparative study. J Mol Evol 63: 120-126, 2006.
84. Wang J, Zhao C, Meng B, Xie J, Zhou C, Chen X, Zhao K, Shao J, Xue Y, Xu N, Ma Y, Liu S. The proteomic alterations of Thermoanaerobacter tengcongensis cultured at different temperatures. Proteomics 7: 1409-1419, 2007.
85. Wang Z, Tong W, Wang Q, Bai X, Chen Z, Zhao J, Xu N, Liu S. The temperature dependent proteomic analysis of Thermotoga maritima. PLos One 7: e46463, 2012.
86. Wilson CM, Yang S, Rodriguez M Jr, Ma Q, Johnson CM, Dice L, Xu Y, Brown SD. Clostridium thermocellum transcriptomic profiles after exposure to furfural or heat stress. Biotechnol Biofuels 6: 131, 2013.
87. Yangala K, Suryanarayana T. Studies on structural stability of thermophilic Sulfolobus acidocaldarius ribosomes. Indian J Biochem Biophys 44: 19-25, 2007.
88. Yoon SH, Reiss DJ, Bare JC, Tenenbaum D, Pan M, Slagel J, Moritz RL, Lim S, Hackett M, Menon AL, Adams MW, Barnebey A, Yannone SM, Leigh JA, Baliga NS. Parallel evolution of transcriptome architecture during genome reorganization. Genome Res 21: 1892-1904, 2011.
89. Yun SH, Choi CW, Kwon SO, Lee YG, Chung YH, Jung HJ, Kim YJ, Lee JH, Choi JS, Kim S, Kim SI. Enrichment and proteome analysis of a hyperthermostable protein set of archaeon Thermococcus onnurineus NA1. Extremophiles 15: 451- 461, 2011.
90. Zeldovich KB, Berezovsky IN, Shakhnovich EI. Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput Biol 3: e5, 2007.