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Extremophilic Enzymes Related to Energy Conversion

  • Satoshi Wakai
  • Yoshihiro Sambongi
Chapter

Abstract

Across the Earth, a variety of organisms inhabit both mild and extreme environments wherever liquid water is available. Among these, extremophilic microorganisms, termed extremophiles, favorably live in extreme environments by adapting their physiological properties. Such extremophiles must acquire energy in order to maintain their cell homeostasis, which is functionally similar to organisms living in mild environments. Numerous enzyme proteins from extremophiles such as thermophiles, psychrophiles, piezophiles, and halophiles have been investigated to date, revealing both unity and diversity in their biochemical and structural biological features through comparison with their homologous counterpart enzymes from organisms living in mild environments. In this chapter, we aim to summarize the biochemical and thermodynamic aspects of enzymes related to the energy conversion that occurs in extremophiles. The obtained insights into extremophilic enzymes related to energy conversion thereby allow us to decipher the mechanistic fundamentals of these protein machineries.

Keywords

Extremophile Enzyme Energy conversion Biochemistry Thermodynamics 

References

  1. Adams MW, Perler FB, Kelly RM (1995) Extremozymes: expanding the limits of biocatalysis. Nat Biotechnol 13(7):662–668CrossRefGoogle Scholar
  2. Amend JP, Plyasunov AV (2001) Carbohydrates in thermophile metabolism: calculation of the standard molal thermodynamic properties of aqueous pentoses and hexoses at elevated temperatures and pressures. Geochim Cosmochima Acta 65:3901–3917CrossRefGoogle Scholar
  3. Amend JP, Shock EL (2001) Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol Rev 25:175–243PubMedCrossRefGoogle Scholar
  4. Boujelben I, Gomariz M, Martínez-García M, Santos F, Peña A, López C, Antón J, Maalej S (2012) Spatial and seasonal prokaryotic community dynamics in ponds of increasing salinity of Sfax solar saltern in Tunisia, vol 101. Antonie Van Leeuwenhoek, pp 845–857PubMedCrossRefGoogle Scholar
  5. Bianconi ML (2003) Calorimetric determination of thermodynamic parameters of reaction reveals different enthalpic compensations of the yeast hexokinase isozymes. J Biol Chem 278:18709–18713PubMedCrossRefGoogle Scholar
  6. Bischoff JL, Rosenbauer JR (1988) Liquid-vapor relations in the critical region of the system NaCl-H2O from 380 to 415 °C: a refined determination of the critical point and two-phase boundary of seawater. Geochim Cosmochim Acta 52:2121–2126CrossRefGoogle Scholar
  7. Boonyaratanakornkit BB, Park CB, Clark DS (2002) Pressure effects on intra- and intermolecular interactions within proteins. Biochim Biophys Acta 1595:235–249PubMedCrossRefGoogle Scholar
  8. Bozal N, Montes MJ, Tudela E, Jiménez F, Guinea J (2002) Shewanella frigidimarina and Shewanella livingstonensis sp. nov. isolated from Antarctic coastal areas. Int J Syst Evol Microbiol 52:195–205PubMedCrossRefGoogle Scholar
  9. Cacciapuoti G, Porcelli M, Bertoldo C, De Rosa M, Zappia V (1994) Purification and characterization of extremely thermophilic and thermostable 5’-methylthioadenosine phosphorylase from the archaeon Sulfolobus solfataricus. Purine nucleoside phosphorylase activity and evidence for intersubunit disulfide bonds. J Biol Chem 269:24762–24769PubMedGoogle Scholar
  10. Cacciapuoti G, Fuccio F, Petraccone L, Del Vecchio P, Porcelli M (2012) Role of disulfide bonds in conformational stability and folding of 5’-deoxy-5’-methylthioadenosine phosphorylase II from the hyperthermophilic archaeon Sulfolobus solfataricus. Biochim Biophys Acta 1824:1136–1143PubMedCrossRefGoogle Scholar
  11. Chan CH, Yu TH, Wong KB (2011) Stabilizing Salt-bridge enhances protein thermostability by reducing the heat capacity change of unfolding. PLoS ONE 6(6):e21624PubMedPubMedCentralCrossRefGoogle Scholar
  12. Christian JH, Waltho JA (1962) Solute concentrations within cells of halophilic and non-halophilic bacteria. Biochim Biophys Acta 17:506–508CrossRefGoogle Scholar
  13. Consonni R, Santomo L, Fusi P, Tortora P, Zetta L (1999) A single-point mutation in the extreme heat- and pressure-resistant sso7d protein from Sulfolobus solfataricus leads to a major rearrangement of the hydrophobic core. Biochemistry 38:12709–12717PubMedCrossRefGoogle Scholar
  14. Czop M, Motyka J, Sracek O, Szuwarzyński M (2011) Geochemistry of the hyperalkaline Gorka pit lake (pH > 13) in the Chrzanow region, southern Poland. Water Air Soil Pollution 214:423–434CrossRefGoogle Scholar
  15. D’Amico S, Sohier JS, Feller G (2006) Kinetics and energetics of ligand binding determined by microcalorimetry: insights into active site mobility in a psychrophilic alpha-amylase. J Mol Biol 358:1296–1304PubMedCrossRefGoogle Scholar
  16. de Meis L (1989) Role of water in the energy of hydrolysis of phosphate compounds—energy transduction in biological membranes. Biochim Biophys Acta 973:333–349PubMedCrossRefGoogle Scholar
  17. Demirjian DC, Morís-Varas F, Cassidy CS (2001) Enzymes from extremophiles. Curr Opin Chem Biol 5:144–151PubMedCrossRefGoogle Scholar
  18. Di Giulio M (2005) A comparison of proteins from Pyrococcus furiosus and Pyrococcus abyssi: barophily in the physicochemical properties of amino acids and in the genetic code. Gene 346:1–6PubMedCrossRefGoogle Scholar
  19. Dubnovitsky AP, Kapetaniou EG, Papageorgiou AC (2005) Enzyme adaptation to alkaline pH: atomic resolution (1.08 Å) structure of phosphoserine aminotransferase from Bacillus alcalophilus. Protein Sci 14:97–110PubMedPubMedCentralCrossRefGoogle Scholar
  20. Evilia C, Hou YM (2006) Acquisition of an insertion peptide for efficient aminoacylation by a halophile tRNA synthetase. Biochemistry 45:6835–6845PubMedCrossRefGoogle Scholar
  21. Feller G (2007) Life at low temperatures: is disorder the driving force? Extremophiles 11:211–216PubMedCrossRefGoogle Scholar
  22. Feller G (2010) Protein stability and enzyme activity at extreme biological temperatures. J Phys Condens Matter 22:323101PubMedCrossRefGoogle Scholar
  23. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208PubMedCrossRefGoogle Scholar
  24. Frolow F, Harel M, Sussman JL, Mevarech M, Shoham M (1996) Insights into protein adaptation to a saturated salt environment from the crystal structure of a halophilic 2Fe-2S ferredoxin. Nat Struct Biol 3:452–458PubMedCrossRefGoogle Scholar
  25. Fujii S, Oki H, Kawahara K, Yamane D, Yamanaka M, Maruno T, Kobayashi Y, Masanari M, Wakai S, Nishihara H, Ohkubo T, Sambongi Y (2017) Structural and functional insights into thermally stable cytochrome c’ from a thermophile. Protein Sci 26:737–748PubMedPubMedCentralCrossRefGoogle Scholar
  26. Fukuchi S, Nishikawa K (2001) Protein surface amino acid compositions distinctively differ between thermophilic and mesophilic bacteria. J Mol Biol 309:835–843PubMedCrossRefGoogle Scholar
  27. George P, Witonsky RJ, Trachtman M, Wu C, Dorwart W, Richman L, Richman W, Shurayh F, Lentz B (1970) “Squiggle-H2O”. An enquiry into the importance of solvation effects in phosphate ester and anhydride reactions. Biochim Biophys Acta 223:1–15PubMedPubMedCentralCrossRefGoogle Scholar
  28. Goto E, Kodama T, Minoda Y (1978) Growth and taxonomy of thermophilic hydrogen bacteria. Agric Biol Chem 42:1305–1308Google Scholar
  29. Graziano G, Merlino A (2014) Molecular bases of protein halotolerance. Biochim Biophys Acta 1844:850–858PubMedCrossRefGoogle Scholar
  30. Hakamada S, Sonoyama T, Ichiki S, Nakamura S, Uchiyama S, Kobayashi Y, Sambongi Y (2008) Stabilization mechanism of cytochrome c552 from a moderately thermophilic bacterium, Hydrogenophilus thermoluteolus. Biosci Biotechnol Biochem 72:2103–2109PubMedCrossRefGoogle Scholar
  31. Hallsworth JE, Yakimov MM, Golyshin PN, Gillion JL, D’Auria G, de Lima Alves F, La Cono V, Genovese M, McKew BA, Hayes SL, Harris G, Giuliano L, Timmis KN, McGenity TJ (2007) Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ Microbiol 9:801–813PubMedCrossRefGoogle Scholar
  32. Hara KY, Araki M, Okai N, Wakai S, Hasunuma T, Kondo A (2014) Development of bio-based fine chemical production through synthetic bioengineering. Microb Cell Fact 13:173PubMedPubMedCentralCrossRefGoogle Scholar
  33. Harrison JP, Gheeraert N, Tsigelnitskiy D, Cockell CS (2013) The limits for life under multiple extremes. Trends Microbiol 21:204–212PubMedCrossRefGoogle Scholar
  34. Hasegawa J, Uchiyama S, Tanimoto Y, Mizutani M, Kobayashi Y, Sambongi Y, Igarashi Y (2000) Selected mutations in a mesophilic cytochrome c confer the stability of a thermophilic counterpart. J Biol Chem 275:37824–37828PubMedCrossRefGoogle Scholar
  35. Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61:237–258PubMedCrossRefGoogle Scholar
  36. Hoehler TM (2007) An energy balance concept for habitability. Astrobiology 7:824–838PubMedCrossRefGoogle Scholar
  37. Hong J, Yoshida N, Chong SH, Lee C, Ham S, Hirata F (2012) Elucidating the molecular origin of hydrolysis energy of pyrophosphate in water. J Chem Theory Comput 8:2239–2246PubMedPubMedCentralCrossRefGoogle Scholar
  38. Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol Rev 63:735–750PubMedPubMedCentralGoogle Scholar
  39. Huang Y, Krauss G, Cottaz S, Driguez H, Lipps G (2005) A highly acid-stable and thermostable endo-beta-glucanase from the thermoacidophilic archaeon Sulfolobus solfataricus. Biochem J 385:581–588PubMedPubMedCentralCrossRefGoogle Scholar
  40. Jetten MS, Stams AJ, Zehnder AJ (1989) Isolation and characterization of acetyl-coenzyme A synthetase from Methanothrix soehngenii. J Bacteriol 171:5430–5435PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kanao T, Matsumoto C, Shiraga K, Yoshida K, Takada J, Kamimura K (2010) Recombinant tetrathionate hydrolase from Acidithiobacillus ferrooxidans requires exposure to acidic conditions for proper folding. FEMS Microbiol Lett 309:43–47PubMedGoogle Scholar
  42. Kang X, Carey J (1999) Role of heme in structural organization of cytochrome c probed by semisynthesis. Biochemistry 38:15944–15951PubMedCrossRefGoogle Scholar
  43. Kankare J, Salminen T, Lahti R, Cooperman BS, Baykov AA, Goldman A (1996) Structure of Escherichia coli inorganic pyrophosphatase at 2.2 A resolution. Acta Crystallogr D Biol Crystallogr 52:551–563PubMedCrossRefGoogle Scholar
  44. Karan R, Capes MD, DasSarma S (2012) Function and biotechnology of extremophilic enzymes in low water activity. Aquat Biosyst 8(1):4PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kastritis PL, Papandreou NC, Hamodrakas SJ (2007) Haloadaptation: insights from comparative modeling studies of halophilic archaeal DHFRs. Int J Biol Macromol 41:447–453PubMedCrossRefGoogle Scholar
  46. Kato Y, Fujii S, Kuribayashi TA, Masanari M, Sambongi Y (2015) Thermal stability of cytochrome c’ from mesophilic Shewanella amazonensis. Biosci Biotechnol Biochem 79:1125–1129PubMedCrossRefGoogle Scholar
  47. Kato C, Li L, Nogi Y, Nakamura Y, Tamaoka J, Horikoshi K (1998) Extremely barophilic bacteria isolated from the Mariana Trench, Challenger Deep, at a depth of 11,000 meters. Appl Environ Microbiol 64:1510–1513PubMedPubMedCentralGoogle Scholar
  48. Kato C, Li L, Tamaoka J, Horikoshi K (1997) Molecular analyses of the sediment of the 11,000-m deep Mariana Trench. Extremophiles 1:117–123PubMedCrossRefGoogle Scholar
  49. Kato C, Nogi Y (2001) Correlation between phylogenetic structure and function: examples from deep-sea Shewanella. FEMS Microbiol Ecol 35:223–230PubMedCrossRefGoogle Scholar
  50. Kimura K, Morimatsu K, Inaoka T, Yamamoto K (2017) Injury and recovery of Escherichia coli ATCC25922 cells treated by high hydrostatic pressure at 400–600 MPa. J Biosci Bioeng 123:698–706PubMedCrossRefGoogle Scholar
  51. Kobayashi S, Fujii S, Koga A, Wakai S, Matubayasi N, Sambongi Y (2017) Pseudomonas aeruginosa cytochrome c551 denaturation by five systematic urea derivatives that differ in the alkyl chain length. Biosci Biotechnol Biochem 81:1274–1278PubMedCrossRefGoogle Scholar
  52. Koschinsky A, Garbe-Schönberg D, Sander S, Schmidt K, Gennerich HH, Strauss H (2008) Hydrothermal venting at pressure-temperature conditions above the critical point of seawater, 5 S on the Mid-Atlantic Ridge. Geology 36:615–618CrossRefGoogle Scholar
  53. Kumari S, Tishel R, Eisenbach M, Wolfe AJ (1995) Cloning, characterization, and functional expression of acs, the gene which encodes acetyl coenzyme A synthetase in Escherichia coli. J Bacteriol 177:2878–2886PubMedPubMedCentralCrossRefGoogle Scholar
  54. Kuribayashi TA, Fujii S, Masanari M, Yamanaka M, Wakai S, Sambongi Y (2017) Difference in NaCl tolerance of membrane-bound 5’-nucleotidases purified from deep-sea and brackish water Shewanella species. Extremophiles 21:357–368PubMedCrossRefGoogle Scholar
  55. Kushner DJ (1993) Growth and nutrition of halophilic bacteria. In: Vreeland RH, Hochstein L (eds) The biology of halophilic bacteria. CRC Press, Boca Raton, FL, pp 87–103Google Scholar
  56. Kusube M, Kyaw TS, Tanikawa K, Chastain RA, Hardy KM, Cameron J, Bartlett DH (2017) Colwellia marinimaniae sp. nov., a hyperpiezophilic species isolated from an amphipod within the Challenger Deep, Mariana Trench. Int J Syst Evol Microbiol 67:824–831PubMedCrossRefGoogle Scholar
  57. Lavire C, Normand P, Alekhina I, Bulat S, Prieur D, Birrien JL, Fournier P, Hänni C, Petit JR (2006) Presence of Hydrogenophilus thermoluteolus DNA in accretion ice in the subglacial Lake Vostok, Antarctica, assessed using rrs, cbb and hox. Environ Microbiol 8:2106–2114PubMedCrossRefGoogle Scholar
  58. Lee CF, Makhatadze GI, Wong KB (2005) Effects of charge-to-alanine substitutions on the stability of ribosomal protein L30e from Thermococcus celer. Biochemistry 44:16817–16825PubMedCrossRefGoogle Scholar
  59. Leppänen VM, Nummelin H, Hansen T, Lahti R, Schäfer G, Goldman A (1999) Sulfolobus acidocaldarius inorganic pyrophosphatase: structure, thermostability, and effect of metal ion in an archael pyrophosphatase. Protein Sci 8:1218–1231PubMedPubMedCentralCrossRefGoogle Scholar
  60. Liu B, Bartlam M, Gao R, Zhou W, Pang H, Liu Y, Feng Y, Rao Z (2004) Crystal structure of the hyperthermophilic inorganic pyrophosphatase from the archaeon Pyrococcus horikoshii. Biophys J 86:420–427PubMedPubMedCentralCrossRefGoogle Scholar
  61. Madern D, Ebel C (2007) Influence of an anion-binding site in the stabilization of halophilic malate dehydrogenase from Haloarcula marismortui. Biochimie 89:981–987PubMedCrossRefGoogle Scholar
  62. Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91–98PubMedCrossRefGoogle Scholar
  63. Mancinelli R, Botti A, Bruni F, Ricci MA, Soper AK (2007) Hydration of sodium, potassium, and chloride ions in solution and the concept of structure maker/breaker. J Phys Chem B 111:13570–13577PubMedCrossRefGoogle Scholar
  64. Marg BL, Schweimer K, Sticht H, Oesterhelt D (2005) A two-alpha-helix extra domain mediates the halophilic character of a plant-type ferredoxin from halophilic archaea. Biochemistry 44:29–39PubMedCrossRefGoogle Scholar
  65. Masanari M, Fujii S, Kawahara K, Oki H, Tsujino H, Maruno T, Kobayashi Y, Ohkubo T, Wakai S, Sambongi Y (2016) Comparative study on stabilization mechanism of monomeric cytochrome c5 from deep-sea piezophilic Shewanella violacea. Biosci Biotechnol Biochem 80:2365–2370PubMedCrossRefGoogle Scholar
  66. Masanari M, Wakai S, Ishida M, Kato C, Sambongi Y (2014) Correlation between the optimal growth pressures of four Shewanella species and the stabilities of their cytochromes c5. Extremophiles 18:617–627PubMedCrossRefGoogle Scholar
  67. Masanari M, Wakai S, Tamegai H, Kurihara T, Kato C, Sambongi Y (2011) Thermal stability of cytochrome c5 of pressure-sensitive Shewanella livingstonensis. Biosci Biotechnol Biochem 75:1859–1861PubMedCrossRefGoogle Scholar
  68. Mayer F, Küper U, Meyer C, Daxer S, Müller V, Rachel R, Huber H (2012) AMP-forming acetyl coenzyme A synthetase in the outermost membrane of the hyperthermophilic crenarchaeon Ignicoccus hospitalis. J Bacteriol 194:1572–1581PubMedPubMedCentralCrossRefGoogle Scholar
  69. McMillan LJ, Hepowit NL, Maupin-Furlow JA (2015) Archaeal inorganic pyrophosphatase displays robust activity under high-salt conditions and in organic solvents. Appl Environ Microbiol 82:538–548PubMedCrossRefGoogle Scholar
  70. Médicis ED, Paquette J, Gauthier JJ, Shapcott D (1986) Magnesium and manganese content of halophilic bacteria. Appl Environ Microbiol 52:567–573PubMedPubMedCentralGoogle Scholar
  71. Mevarech M, Frolow F, Gloss LM (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86:155–164PubMedCrossRefGoogle Scholar
  72. Miyashita Y, Ohmae E, Nakasone K, Katayanagi K (2015) Effects of salt on the structure, stability, and function of a halophilic dihydrofolate reductase from a hyperhalophilic archaeon, Haloarcula japonica strain TR-1. Extremophiles 19:479–493PubMedCrossRefGoogle Scholar
  73. Morin PE, Freire E (1991) Direct calorimetric analysis of the enzymatic activity of yeast cytochrome c oxidase. Biochemistry 30:8494–8500PubMedCrossRefGoogle Scholar
  74. Morozkina EV, Slutskaya ES, Fedorova TV, Tugay TI, Golubeva LI, Koroleva OV (2010) Extremophilic microorganisms: biochemical adaptation and biotechnological application. Appl Biochem Microbiol 46:1–14CrossRefGoogle Scholar
  75. Mykytczuk NC, Foote SJ, Omelon CR, Southam G, Greer CW, Whyte LG (2013) Bacterial growth at −15 °C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7:1211–1226PubMedPubMedCentralCrossRefGoogle Scholar
  76. Nakamura S, Ichiki S, Takashima H, Uchiyama S, Hasegawa J, Kobayashi Y, Sambongi Y, Ohkubo T (2006) Structure of cytochrome c552 from a moderate thermophilic bacterium, Hydrogenophilus thermoluteolus: comparative study on the thermostability of cytochrome c. Biochemistry 45:6115–6123PubMedCrossRefGoogle Scholar
  77. Nealson KH, Rowe AR (2016) Electromicrobiology: realities, grand challenges, goals and predictions. Microb Biotechnol 9:595–600PubMedPubMedCentralCrossRefGoogle Scholar
  78. Nogi Y, Kato C, Horikoshi K (1998) Taxonomic studies of deep-sea barophilic Shewanella strains and description of Shewanella violacea sp. nov. Arch Microbiol 170:331–338PubMedCrossRefGoogle Scholar
  79. Obuchi M, Kawahara K, Motooka D, Nakamura S, Yamanaka M, Takeda T, Uchiyama S, Kobayashi Y, Ohkubo T, Sambongi Y (2009) Hyperstability and crystal structure of cytochrome c555 from hyperthermophilic Aquifex aeolicus. Acta Crystallogr D Biol Crystallogr 65:804–813PubMedCrossRefGoogle Scholar
  80. Oda K, Kodama R, Yoshidome T, Yamanaka M, Sambongi Y, Kinoshita M (2011) Effects of heme on the thermal stability of mesophilic and thermophilic cytochromes c: comparison between experimental and theoretical results. J Chem Phys 134:025101PubMedPubMedCentralCrossRefGoogle Scholar
  81. Ogawa K, Sonoyama T, Takeda T, Ichiki S, Nakamura S, Kobayashi Y, Uchiyama S, Nakasone K, Takayama SJ, Mita H, Yamamoto Y, Sambongi Y (2007) Roles of a short connecting disulfide bond in the stability and function of psychrophilic Shewanella violacea cytochrome c5. Extremophiles 11:797–807PubMedCrossRefGoogle Scholar
  82. Ohshida T, Hayashi J, Satomura T, Kawakami R, Ohshima T, Sakuraba H (2016) First characterization of extremely halophilic 2-deoxy-D-ribose-5-phosphate aldolase. Protein Expr Purif 126:62–68PubMedCrossRefGoogle Scholar
  83. Oikawa K, Nakamura S, Sonoyama T, Ohshima A, Kobayashi Y, Takayama SJ, Yamamoto Y, Uchiyama S, Hasegawa J, Sambongi Y (2005) Five amino acid residues responsible for the high stability of Hydrogenobacter thermophilus cytochrome c552: reciprocal mutation analysis. J Biol Chem 280:5527–5532PubMedCrossRefGoogle Scholar
  84. Onodera M, Yatsunami R, Tsukimura W, Fukui T, Nakasone K, Takashina T, Nakamura S (2013) Gene analysis, expression, and characterization of an intracellular α-amylase from the extremely halophilic archaeon Haloarcula japonica. Biosci Biotechnol Biochem 77:281–288PubMedCrossRefGoogle Scholar
  85. Oren A (1983) Halobacterium sodomense sp. nov., a dead sea halobacterium with an extremely high magnesium requirement. Int J Syst Evol Microbiol 33:381–386CrossRefGoogle Scholar
  86. Oren A (2013) Life at high salt concentrations, intracellular KCl concentrations, and acidic proteomes. Front Microbiol 4:315PubMedPubMedCentralCrossRefGoogle Scholar
  87. Ozawa K, Harashina T, Yatsunami R, Nakamura S (2005) Gene cloning, expression and partial characterization of cell division protein FtsZ1 from extremely halophilic archaeon Haloarcula japonica strain TR-1. Extremophiles 9:281–288PubMedCrossRefGoogle Scholar
  88. Popinako A, Antonov M, Tikhonov A, Tikhonova T, Popov V (2017) Structural adaptations of octaheme nitrite reductases from haloalkaliphilic Thioalkalivibrio bacteria to alkaline pH and high salinity. PLoS ONE 12:e0177392PubMedPubMedCentralCrossRefGoogle Scholar
  89. Romero PJ, de Meis L (1989) Role of water in the energy of hydrolysis of phosphoanhydride and phosphoester bonds. J Biol Chem 264:7869–7873PubMedGoogle Scholar
  90. Rosenbaum E, Gabel F, Durá MA, Finet S, Cléry-Barraud C, Masson P, Franzetti B (2012) Effects of hydrostatic pressure on the quaternary structure and enzymatic activity of a large peptidase complex from Pyrococcus horikoshii. Arch Biochem Biophys 517:104–110PubMedCrossRefGoogle Scholar
  91. Saint-Martin H, Ortega-Blake I, Leś A, Adamowicz L (1994) The role of hydration in the hydrolysis of pyrophosphate. A Monte Carlo simulation with polarizable-type interaction potentials. Biochim Biophys Acta 1207:12–23PubMedCrossRefGoogle Scholar
  92. Sarethy IP, Saxena Y, Kapoor A, Sharma M, Sharma SK, Gupta V, Gupta S (2011) Alkaliphilic bacteria: applications in industrial biotechnology. J Ind Microbiol Biotechnol 38:769–790PubMedCrossRefGoogle Scholar
  93. Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403–433PubMedCrossRefGoogle Scholar
  94. Stetter KO (1999) Extremophiles and their adaptation to hot environments. FEBS Lett 452:22–25PubMedCrossRefGoogle Scholar
  95. Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280PubMedPubMedCentralGoogle Scholar
  96. Schleper C, Pühler G, Kühlmorgen B, Zillig W (1995a) Life at extremely low pH. Nature 375:741–742PubMedCrossRefGoogle Scholar
  97. Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U, Klenk HP, Zillig W (1995b) Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol 177:7050–7059PubMedPubMedCentralCrossRefGoogle Scholar
  98. Sharma A, Kawarabayasi Y, Satyanarayana T (2012) Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16:1–19PubMedCrossRefGoogle Scholar
  99. Siglioccolo A, Paiardini A, Piscitelli M, Pascarella S (2011) Structural adaptation of extreme halophilic proteins through decrease of conserved hydrophobic contact surface. BMC Struct Biol 11:50PubMedPubMedCentralCrossRefGoogle Scholar
  100. Siliakus MF, van der Oost J, Kengen SWM (2017) Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure. Extremophiles 21:651–670PubMedPubMedCentralCrossRefGoogle Scholar
  101. Soppa J (2006) From genomes to function: haloarchaea as model organisms. Microbiology 152:585–590PubMedCrossRefGoogle Scholar
  102. Sun MM, Caillot R, Mak G, Robb FT, Clark DS (2001) Mechanism of pressure-induced thermostabilization of proteins: studies of glutamate dehydrogenases from the hyperthermophile Thermococcus litoralis. Protein Sci 10:1750–1757PubMedPubMedCentralCrossRefGoogle Scholar
  103. Tadeo X, López-Méndez B, Trigueros T, Laín A, Castaño D, Millet O (2009) Structural basis for the aminoacid composition of proteins from halophilic archea. PLoS Biol 7:e1000257PubMedPubMedCentralCrossRefGoogle Scholar
  104. Takai K, Gamo T, Tsunogai U, Nakayama N, Hirayama H, Nealson KH, Horikoshi K (2004) Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field. Extremophiles 8:269–282PubMedCrossRefGoogle Scholar
  105. Takai K, Moser DP, Onstott TC, Spoelstra N, Pfiffner SM, Dohnalkova A, Fredrickson JK (2001) Alkaliphilus transvaalensis gen. nov., sp. nov., an extremely alkaliphilic bacterium isolated from a deep South African gold mine. Int J Syst Evol Microbiol 51:1245–1256PubMedCrossRefGoogle Scholar
  106. Takai K, Nakamura K, Toki T, Tsunogai U, Miyazaki M, Miyazaki J, Hirayama H, Nakagawa S, Nunoura T, Horikoshi K (2008) Cell proliferation at 122 °C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc Natl Acad Sci U S A 105:10949–10954PubMedPubMedCentralCrossRefGoogle Scholar
  107. Takeda T, Sonoyama T, Takayama SJ, Mita H, Yamamoto Y, Sambongi Y (2009) Correlation between the stability and redox potential of three homologous cytochromes c from two thermophiles and one mesophile. Biosci Biotechnol Biochem 73:366–371PubMedCrossRefGoogle Scholar
  108. Takenaka S, Wakai S, Tamegai H, Uchiyama S, Sambongi Y (2010) Comparative analysis of highly homologous Shewanella cytochromes c5 for stability and function. Biosci Biotechnol Biochem 74:1079–1083PubMedCrossRefGoogle Scholar
  109. Taupin CM, Härtlein M, Leberman R (1997) Seryl-tRNA synthetase from the extreme halophile Haloarcula marismortui–isolation, characterization and sequencing of the gene and its expression in Escherichia coli. Eur J Biochem 243:141–150PubMedCrossRefGoogle Scholar
  110. Teplyakov A, Obmolova G, Wilson KS, Ishii K, Kaji H, Samejima T, Kuranova I (1994) Crystal structure of inorganic pyrophosphatase from Thermus thermophilus. Protein Sci 3:1098–1107PubMedPubMedCentralCrossRefGoogle Scholar
  111. Todd MJ, Gomez J (2001) Enzyme kinetics determined using calorimetry: a general assay for enzyme activity? Anal Biochem 296:179–187PubMedCrossRefGoogle Scholar
  112. van der Wielen PW, Bolhuis H, Borin S, Daffonchio D, Corselli C, Giuliano L, D’Auria G, de Lange GJ, Huebner A, Varnavas SP, Thomson J, Tamburini C, Marty D, McGenity TJ, Timmis KN, Party BioDeep Scientific (2005) The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307:121–123PubMedCrossRefGoogle Scholar
  113. Venkateswaran K, Dollhopf ME, Aller R, Stackebrandt E, Nealson KH (1998) Shewanella amazonensis sp. nov., a novel metal-reducing facultative anaerobe from Amazonian shelf muds. Int J Syst Bacteriol 48:965–972PubMedCrossRefGoogle Scholar
  114. Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65:1–43PubMedPubMedCentralCrossRefGoogle Scholar
  115. Wakai S, Abe A, Fujii S, Nakasone K, Sambongi Y (2017a) Pyrophosphate hydrolysis in the extremely halophilic archaeon Haloarcula japonica is catalyzed by a single enzyme with a broad ionic strength range. Extremophiles 21:471–477PubMedCrossRefGoogle Scholar
  116. Wakai S, Arazoe T, Ogino C, Kondo A (2017b) Future insights in fungal metabolic engineering. Bioresour Technol 245(Pt B):1314–1326PubMedCrossRefGoogle Scholar
  117. Wakai S, Masanari M, Ikeda T, Yamaguchi N, Ueshima S, Watanabe K, Nishihara H, Sambongi Y (2013a) Oxidative phosphorylation in a thermophilic, facultative chemoautotroph, Hydrogenophilus thermoluteolus, living prevalently in geothermal niches. Environ Microbiol Rep 5:235–242PubMedCrossRefGoogle Scholar
  118. Wakai S, Kidokoro S, Masaki K, Nakasone K, Sambongi Y (2013b) Constant enthalpy change value during pyrophosphate hydrolysis within the physiological limits of NaCl. J Biol Chem 288:29247–29251PubMedPubMedCentralCrossRefGoogle Scholar
  119. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95:6578–6583PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wolfenden R (2006) Degrees of difficulty of water-consuming reactions in the absence of enzymes. Chem Rev 106:3379–3396PubMedCrossRefGoogle Scholar
  121. Yamanaka M, Masanari M, Sambongi Y (2011) Conferment of folding ability to a naturally unfolded apocytochrome c through introduction of hydrophobic amino acid residues. Biochemistry 50:2313–2320PubMedCrossRefGoogle Scholar
  122. Yamanaka M, Mita H, Yamamoto Y, Sambongi Y (2009) Heme is not required for Aquifex aeolicus cytochrome c555 polypeptide folding. Biosci Biotechnol Biochem 73:2022–2025PubMedCrossRefGoogle Scholar
  123. Zhang G, Ge H (2013) Protein hypersaline adaptation: insight from amino acids with machine learning algorithms. Protein J 32:239–245PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Graduate School of Science, Technology, and InnovationKobe UniversityKobeJapan
  2. 2.Graduate School of Biosphere ScienceHiroshima UniversityHiroshimaJapan

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