Skip to main content
Log in

Thermus thermophilus as biological model

  • Review
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Thermus spp is one of the most wide spread genuses of thermophilic bacteria, with isolates found in natural as well as in man-made thermal environments. The high growth rates, cell yields of the cultures, and the constitutive expression of an impressively efficient natural competence apparatus, amongst other properties, make some strains of the genus excellent laboratory models to study the molecular basis of thermophilia. These properties, together with the fact that enzymes and protein complexes from extremophiles are easier to crystallize have led to the development of an ongoing structural biology program dedicated to T. thermophilus HB8, making this organism probably the best so far known from a protein structure point view. Furthermore, the availability of plasmids and up to four thermostable antibiotic selection markers allows its use in physiological studies as a model for ancient bacteria. Regarding biotechnological applications this genus continues to be a source of thermophilic enzymes of great biotechnological interest and, more recently, a tool for the over-expression of thermophilic enzymes or for the selection of thermostable mutants from mesophilic proteins by directed evolution. In this article, we review the properties of this organism as biological model and its biotechnological applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alarico S, Empadinhas N, Simoes C, Silva Z, Henne A, Mingote A, Santos H, da Costa MS (2005) Distribution of genes for synthesis of trehalose and Mannosylglycerate in Thermus spp. and direct correlation of these genes with halotolerance. Appl Environ Microbiol 71:2460–2466

    PubMed  CAS  Google Scholar 

  • Alarico S, Empadinhas N, Mingote A, Simoes C, Santos MS, da Costa MS (2007) Mannosylglycerate is essential for osmotic adjustment in Thermus thermophilus strains HB27 and RQ-1. Extremophiles 11:833–840

    PubMed  CAS  Google Scholar 

  • Albers SV, Jonuscheit M, Dinkelaker S, Urich T, Kletzin A, Tampe R, Driessen AJ, Schleper C (2006) Production of recombinant and tagged proteins in the hyperthermophilic archaeon Sulfolobus solfataricus. Appl Environ Microbiol 72:102–111

    PubMed  CAS  Google Scholar 

  • Anderson R, Huang Y (1992) Fatty acids are precursors of alkylamines in Deinococcus radiodurans. J Bacteriol 174:7168–7173

    PubMed  CAS  Google Scholar 

  • Angelini S, Moreno R, Gouffi K, Santini C-L, Yamagishi A, Berenguer J, Wu L-F (2001) Export of Thermus thermophilus alkaline phosphatase via the twin-arginine translocation pathway in Escherichia coli. FEBS Lett 506:103–107

    PubMed  CAS  Google Scholar 

  • Aoki K, Itoh T (2007) Characterization of the ColE2-like replicon of plasmid pTT8 from Thermus thermophilus. Biochem Biophys Res Commun 353:1028–1033

    PubMed  CAS  Google Scholar 

  • Aravalli RN, Garrett RA (1997) Shuttle vectors for hyperthermophilic archaea. Extremophiles 1:183–191

    PubMed  CAS  Google Scholar 

  • Averhoff B (2004) DNA transport and natural transformation in mesophilic and thermophilic bacteria. J Bioenerg Biomembr 36:25–33

    PubMed  CAS  Google Scholar 

  • Barany F (1991) Genetic disease detection and DNA amplification using cloned thermostable ligase. Proc Natl Acad Sci USA 88:189–193

    PubMed  CAS  Google Scholar 

  • Baumeister W, Kubler O, Zingsheim HP (1981) The structure of the cell envelope of Micrococcus radiodurans as revealed by metal shadowing and decoration. J Ultrastruct Res 75:60–71

    PubMed  CAS  Google Scholar 

  • Blas-Galindo E, Cava F, Lopez-Vinas E, Mendieta J, Berenguer J (2007) Use of a dominant rpsL allele conferring streptomycin dependence for positive and negative selection in Thermus thermophilus. Appl Environ Microbiol 73:5138–5145

    PubMed  CAS  Google Scholar 

  • Blondal T, Thorisdottir A, Unnsteinsdottir U, Hjorleifsdottir S, Aevarsson A, Ernstsson S, Fridjonsson OH, Skirnisdottir S, Wheat JO, Hermannsdottir AG, Sigurdsson ST, Hreggvidsson GO, Smith AV, Kristjansson JK (2005) Isolation and characterization of a thermostable RNA ligase 1 from a Thermus scotoductus bacteriophage TS2126 with good single-stranded DNA ligation properties. Nucleic Acids Res 33:135–142

    PubMed  CAS  Google Scholar 

  • Brock TD, Freeze H (1969) Thermus aquaticus gen. n. and sp. n., a non sporulating extreme thermophile. J Bacteriol 98:289–297

    PubMed  CAS  Google Scholar 

  • Brouns SJ, Wu H, Akerboom J, Turnbull AP, de Vos WM, van der Oost J (2005) Engineering a selectable marker for hyperthermophiles. J Biol Chem 280:11422–11431

    PubMed  CAS  Google Scholar 

  • Cannio R, Contursi P, Rossi M, Bartolucci S (2001) Thermoadaptation of a mesophilic hygromycin B phosphotransferase by directed evolution in hyperthermophilic Archaea: selection of a stable genetic marker for DNA transfer into Sulfolobus solfataricus. Extremophiles 5:153–159

    PubMed  CAS  Google Scholar 

  • Castán P (2004) Desarrollo de cepas de interés biotecnológico mediante la manipulación de los genes recA y slpA de Thermus thermophilus. PhD. Thesis. Universidad Autónoma de Madrid

  • Castán P, de Pedro MM, Risco C, Valles C, Fernandez LA, Schwarz H, Berenguer J (2001) Multiple Regulatory Mechanisms Act on the 5′ Untranslated Region of the S-Layer Gene from Thermus thermophilus HB8. J Bacteriol 183:1491–1494

    PubMed  Google Scholar 

  • Castón JR, Berenguer J, de Pedro MA, Carrascosa JL (1993) S-layer protein from Thermus thermophilus HB8 assembles into porin-like structures. Mol Microbiol 9:65–75

    PubMed  Google Scholar 

  • Cava F, Berenguer J (2006) Biochemical and regulatory properties of a respiratory island encoded by a conjugative plasmid in the extreme thermophile Thermus thermophilus. Biochem Soc Trans 34:97–100

    PubMed  CAS  Google Scholar 

  • Cava F, de Pedro MA, Schwarz H, Henne A, Berenguer J (2004a) Binding to pyruvylated compounds as an ancestral mechanism to anchor the outer envelope in primitive bacteria. Mol Microbiol 52:677–690

    PubMed  CAS  Google Scholar 

  • Cava F, Zafra O, Magalon A, Blasco F, Berenguer J (2004b) A new type of NADH dehydrogenase specific for nitrate respiration in the extreme thermophile Thermus thermophilus. J Biol Chem 279:45369–45378

    PubMed  CAS  Google Scholar 

  • Cava F, Laptenko O, Borukhov S, Chahlafi Z, Blas-Galindo E, Gomez-Puertas P, Berenguer J (2007) Control of the respiratory metabolism of Thermus thermophilus by the nitrate respiration conjugative element NCE. Mol Microbiol 64:630–646

    PubMed  CAS  Google Scholar 

  • Cava F, de Pedro MA, Blas-Galindo E, Waldo GS, Westblade LF, Berenguer J (2008a) Expression and use of superfolder green fluorescent protein at high temperatures in vivo: a tool to study extreme thermophile biology. Environ Microbiol 10:605–613

    PubMed  CAS  Google Scholar 

  • Cava F, Zafra O, Berenguer J (2008b) A cytochrome c containing nitrate reductase plays a role in electron transport for denitrification in Thermus thermophilus without involvement of the bc respiratory complex. Mol Microbiol 70:507–518

    PubMed  Google Scholar 

  • Cava F, Zafra O, da Costa MS, Berenguer J (2008c) The role of the nitrate respiration element of Thermus thermophilus in the control and activity of the denitrification apparatus. Environ Microbiol 10:522–533

    PubMed  CAS  Google Scholar 

  • Chautard H, Blas-Galindo E, Menguy T, Grand’Moursel L, Cava F, Berenguer J, Delcourt M (2007) An activity-independent selection system of thermostable protein variants. Nat Methods 4:919–921

    PubMed  CAS  Google Scholar 

  • Chou Q (1992) Minimizing deletion mutagenesis artifact during Taq DNA polymerase PCR by E. coli SSB. Nucleic Acids Res 20:4371

    PubMed  CAS  Google Scholar 

  • Chu SF, Shu HY, Lin LC, Chen MY, Tsay SS, Lin GH (2006) Characterization of a rolling-circle replication plasmid from Thermus aquaticus NTU103. Plasmid 56:46–52

    PubMed  CAS  Google Scholar 

  • Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1286

    PubMed  CAS  Google Scholar 

  • Cline JM, Hogrefe HH (2003) Multi-site mutagenesis. WO2002US22759 20020718

  • Connell SR, Takemoto C, Wilson DN, Wang H, Murayama K, Terada T, Shirouzu M, Rost M, Schuler M, Giesebrecht J, Dabrowski M, Mielke T, Fucini P, Yokoyama S, Spahn CM (2007) Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol Cell 25:751–764

    PubMed  CAS  Google Scholar 

  • Contursi P, Cannio R, Prato S, Fiorentino G, Rossi M, Bartolucci S (2003) Development of a genetic system for hyperthermophilic Archaea: expression of a moderate thermophilic bacterial alcohol dehydrogenase gene in Sulfolobus solfataricus. FEMS Microbiol Lett 218:115–120

    PubMed  CAS  Google Scholar 

  • da Costa MS, Nobre MF, Rainey F (2001) Genus Thermus. Bergey’s Man Syst Bacteriol 1:404–414

    Google Scholar 

  • Dabrowski S, Kur J (1999) Cloning, overexpression and purification of the recombinant His-tagged SSB protein of Escherichia coli and use in polymerase chain reaction amplification. Protein Expr Purif 16:96–102

    PubMed  CAS  Google Scholar 

  • Dabrowski S, Olszewski M, Piatek R, Kur J (2002) Novel thermostable ssDNA-bindin proteins from Thermus thermophilus and Thermus aquaticus -expression and purification. Protein Expr Purif 26:131–138

    PubMed  CAS  Google Scholar 

  • de Grado M, Lasa I, Berenguer J (1998) Characterization of a plasmid replicative origin from an extreme thermophile. FEMS Microbiol Lett 165:51–57

    PubMed  Google Scholar 

  • de Grado M, Castán P, Berenguer J (1999) A high-transformation-efficiency cloning vector for Thermus thermophilus. Plasmid 42:241–245

    PubMed  Google Scholar 

  • Engel AM, Cejka Z, Lupas A, Lottspeich F, Baumeister W (1992) Isolation and cloning of Omp alpha, a coiled-coil protein spanning the periplasmic space of the ancestral eubacterium Thermotoga maritima. EMBO J 11:4369–4378

    PubMed  CAS  Google Scholar 

  • Engelhardt H, Peters J (1998) Structural research on surface layers: a focus on stability, surface layer homology domains, and surface layer-cell wall interactions. J Struct Biol 124:276–302

    PubMed  CAS  Google Scholar 

  • Esteban O, Bernal RA, Donohoe M, Videler H, Sharon M, Robinson CV, Stock D (2008) Stoichiometry and localization of the stator subunits E and G in Thermus thermophilus H + -ATPase/synthase. J Biol Chem 283:2595–2603

    PubMed  CAS  Google Scholar 

  • Fee JA, Yoshida T, Surerus KK, Mather MW (1993) Cytochrome caa3 from the thermophilic bacterium Thermus thermophilus: a member of the heme-copper oxidase superfamily. J Bioenerg Biomembr 25:103–114

    PubMed  CAS  Google Scholar 

  • Fernandez-Herrero LA, Olabarria G, Berenguer J (1997) Surface proteins and a novel transcription factor regulate the expression of the S-layer gene in Thermus thermophilus HB8. Mol Microbiol 24:61–72

    PubMed  CAS  Google Scholar 

  • Ferrin LJ, Camerini-Otero RD (1991) Selective cleavage of human DNA: RecA-assisted restriction endonuclease (RARE) cleavage. Science 254:1494–1497

    PubMed  CAS  Google Scholar 

  • Fridjonsson O, Watzlawick H, Mattes R (2002) Thermoadaptation of alpha-galactosidase AgaB1 in Thermus thermophilus. J Bacteriol 184:3385–3391

    PubMed  CAS  Google Scholar 

  • Friedrich A, Hartsch T, Averhoff B (2001) Natural transformation in mesophilic and thermophilic bacteria: identification and characterization of novel, closely related competence genes in Acinetobacter sp. strain BD413 and Thermus thermophilus HB27. Appl Environ Microbiol 67:3140–3148

    PubMed  CAS  Google Scholar 

  • Friedrich A, Prust C, Hartsch T, Henne A, Averhoff B (2002) Molecular analyses of the natural transformation machinery and identification of pilus structures in the extremely thermophilic bacterium Thermus thermophilus strain HB27. Appl Environ Microbiol 68:745–755

    PubMed  CAS  Google Scholar 

  • Gong N, Chen C, Xie L, Chen H, Lin X, Zhang R (2005) Characterization of a thermostable alkaline phosphatase from a novel species Thermus yunnanensis sp. nov. and investigation of its cobalt activation at high temperature. Biochim Biophys Acta 1750:103–111

    PubMed  CAS  Google Scholar 

  • Griffiths E, Gupta RS (2004) Distinctive protein signatures provide molecular markers and evidence for the monophyletic nature of the Deinococcus-Thermus phylum. J Bacteriol 186:3097–3107

    PubMed  CAS  Google Scholar 

  • Griffiths E, Gupta RS (2007) Identification of signature proteins that are distinctive of the Deinococcus-Thermus phylum. Int Microbiol 10:201–208

    PubMed  CAS  Google Scholar 

  • Gupta RS (2000) The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev 24:367–402

    PubMed  CAS  Google Scholar 

  • Hames C, Halbedel S, Schilling O, Stülke J (2005) Multiple-mutation reaction: a method for simultaneous introduction of multiple mutations into the glpK gene of Myclopasma pneumoniae. Appl Environ Microbiol 71:4097–4100

    PubMed  CAS  Google Scholar 

  • Hansen MR, Blennow A, Pedersen S, Nørgaard L, Engelsen SB (2008) Gel texture and chain structure of amylomaltase-modified starches compared to gelatin. Food Hydrocoll 22:1551–1566

    CAS  Google Scholar 

  • Hellwig P, Soulimane T, Mantele W (2002) Electrochemical, FT-IR and UV/VIS spectroscopic properties of the caa3 oxidase from Thermus thermophilus. Eur J Biochem 269:4830–4838

    PubMed  CAS  Google Scholar 

  • Henne A, Bruggemann H, Raasch C, Wiezer A, Hartsch T, Liesegang H, Johann A, Lienard T, Gohl O, Martinez-Arias R, Jacobi C, Starkuviene V, Schlenczeck S, Dencker S, Huber R, Klenk HP, Kramer W, Merkl R, Gottschalk G, Fritz HJ (2004) The genome sequence of the extreme thermophile Thermus thermophilus. Nat Biotechnol 22:547–553

    PubMed  CAS  Google Scholar 

  • Hidaka Y, Hasegawa M, Nakahara T, Hoshino T (1994) The entire population of Thermus thermophilus cells is always competent at any growth phase. Biosci Biotechnol Biochem 58:1338–1339

    PubMed  CAS  Google Scholar 

  • Hidalgo A, Betancor L, Moreno R, Zafra O, Cava F, Fernandez-Lafuente R, Guisan JM, Berenguer J (2004) Thermus thermophilus as a cell factory for the production of a thermophilic Mn-dependent catalase which fails to be synthesized in an active form in Escherichia coli. Appl Environ Microbiol 70:3839–3844

    PubMed  CAS  Google Scholar 

  • Hoseki J, Yano T, Koyama Y, Kuramitsu S, Kagamiyama H (1999) Directed evolution of thermostable kanamycin-resistance gene: a convenient selection marker for Thermus thermophilus. J Biochem 126:951–956

    PubMed  CAS  Google Scholar 

  • Huang Y, Anderson R (1989) Structure of a novel glucosamine-containing phosphoglycolipid from Deinococcus radiodurans. J Biol Chem 264:18667–18672

    PubMed  CAS  Google Scholar 

  • Jaatinen ST, Happonen LJ, Laurinmaki P, Butcher SJ, Bamford DH (2008) Biochemical and structural characterisation of membrane-containing icosahedral dsDNA bacteriophages infecting thermophilic Thermus thermophilus. Virology 379:10–19

    PubMed  CAS  Google Scholar 

  • Janzon J, Ludwig B, Malatesta F (2007) Electron transfer kinetics of soluble fragments indicate a direct interaction between complex III and the caa3 oxidase in Thermus thermophilus. IUBMB Life 59:563–569

    PubMed  CAS  Google Scholar 

  • Jenney FE Jr, Adams MW (2008) The impact of extremophiles on structural genomics (and vice versa). Extremophiles 12:39–50

    PubMed  CAS  Google Scholar 

  • Jónsson ZO, Thorbjarnardóttir SH, Eggertsson G, Palsdottir A (1994) Sequence of the DNA ligase-encoding gene from Thermus scotoductus and conserved motifs in DNA ligases. Gene 151:177–180

    PubMed  Google Scholar 

  • Jonuscheit M, Martusewitsch E, Stedman KM, Schleper C (2003) A reporter gene system for the hyperthermophilic archaeon Sulfolobus solfataricus based on a selectable and integrative shuttle vector. Mol Microbiol 48:1241–1252

    PubMed  CAS  Google Scholar 

  • Kaminishi T, Wilson DN, Takemoto C, Harms JM, Kawazoe M, Schluenzen F, Hanawa-Suetsugu K, Shirouzu M, Fucini P, Yokoyama S (2007) A snapshot of the 30S ribosomal subunit capturing mRNA via the Shine-Dalgarno interaction. Structure 15:289–297

    PubMed  CAS  Google Scholar 

  • Kayser KJ, Kwak JH, Park HS, Kilbane JJ 2nd (2001) Inducible and constitutive expression using new plasmid and integrative expression vectors for Thermus sp. Lett Appl Microbiol 32:412–418

    PubMed  CAS  Google Scholar 

  • Khan SA (2005) Plasmid rolling-circle replication: highlights of two decades of research. Plasmid 53:126–136

    PubMed  CAS  Google Scholar 

  • Kim JS, Koh S, Kim JJ, Kwon ST, Lee DS (1998) Top DNA polymerase from Thermus thermophilus HB27: gene cloning, sequence determination, and physicochemical properties. Mol Cells 8:157–161

    PubMed  CAS  Google Scholar 

  • Kohda J, Kondo A, Teshima T, Fukuda H, Endo I, T.N·S.K.a.T.Y. (2000) Development of efficient protein refolding systems using chaperonins. In: Progress in Biotechnology. vol 16: Elsevier, Amsterdam, pp 119–124

  • Koyama Y, Hoshino T, Tomizuka N, Furukawa K (1986) Genetic transformation of the extreme thermophile Thermus thermophilus and of other Thermus spp. J Bacteriol 166:338–340

    PubMed  CAS  Google Scholar 

  • Koyama Y, Arikawa Y, Furukawa K (1990a) A plasmid vector for an extreme thermophile, Thermus thermophilus. FEMS Microbiol Lett 72:97–102

    CAS  Google Scholar 

  • Koyama Y, Okamoto S, Furukawa K (1990b) Cloning of α and β-galactosidase genes from an extreme thermophile, Thermus strain T2, and their expresion in Thermus thermophilus. Appl Environ Microbiol 56:2251–2254

    PubMed  CAS  Google Scholar 

  • Lasa I, Castón JR, Fernandez-Herrero LA, de Pedro MA, Berenguer J (1992a) Insertional mutagenesis in the extreme thermophilic eubacteria Thermus thermophilus HB8. Mol Microbiol 6:1555–1564

    PubMed  CAS  Google Scholar 

  • Lasa I, de Grado M, de Pedro MA, Berenguer J (1992b) Development of Thermus-Escherichia shuttle vectors and their use for expression of the Clostridium thermocellum celA gene in Thermus thermophilus. J Bacteriol 174:6424–6431

    PubMed  CAS  Google Scholar 

  • Laurberg M, Asahara H, Korostelev A, Zhu J, Trakhanov S, Noller HF (2008) Structural basis for translation termination on the 70S ribosome. Nature 454:852–857

    PubMed  CAS  Google Scholar 

  • Lee KY, Kim Y-R, Park KH, Lee HG (2006) Effects of [alpha]-glucanotransferase treatment on the thermo-reversibility and freeze-thaw stability of a rice starch gel. Carbohydr Polym 63:347–354

    CAS  Google Scholar 

  • Lee KY, Kim Y-R, Park KH, Lee HG (2008) Rheological and gelation properties of rice starch modified with 4-[alpha]-glucanotransferase. Int J Biol Macromol 42:298–304

    PubMed  CAS  Google Scholar 

  • Li WF, Zhou XX, Lu P (2005) Structural features of thermozymes. Biotechnol Adv 23:271–281

    PubMed  CAS  Google Scholar 

  • Liao H, Mckenzie T, Hageman R (1986) Isolation of a thermoestable enzyme variant by cloning and selection in a thermophile. Proc Natl Acad Sci USA 83:576–580

    PubMed  CAS  Google Scholar 

  • Liebl W (2004) Genomics taken to the extreme. Nat Biotechnol 22:524–525

    PubMed  CAS  Google Scholar 

  • Lioliou EE, Pantazaki AA, Kyriakidis DA (2004) Thermus thermophilus genome analysis: benefits and implications. Microb Cell Fact 3:5–7

    PubMed  Google Scholar 

  • Lu TL, Chen CS, Yang FL, Fung JM, Chen MY, Tsay SS, Li J, Zou W, Wu SH (2004) Structure of a major glycolipid from Thermus oshimai NTU-063. Carbohydr Res 339:2593–2598

    PubMed  CAS  Google Scholar 

  • Lucas S, Toffin L, Zivanovic Y, Charlier D, Moussard H, Forterre P, Prieur D, Erauso G (2002) Construction of a shuttle vector for, and spheroplast transformation of, the hyperthermophilic archaeon Pyrococcus abyssi. Appl Environ Microbiol 68:5528–5536

    PubMed  CAS  Google Scholar 

  • Luo J, Bergstrom DE, Barany F (1996) Improving the fidelity of Thermus thermophilus DNA ligase. Nucleic Acids Res 24:3071–3078

    PubMed  CAS  Google Scholar 

  • Lusetti SL, Cox MM (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem 71:71–100

    PubMed  CAS  Google Scholar 

  • Maier E, Polleichtner G, Boeck B, Schinzel R, Benz R (2001) Identification of the outer membrane porin of Thermus thermophilus HB8: the channel-forming complex has an unusually high molecular mass and an extremely large single-channel conductance. J Bacteriol 183:800–803

    PubMed  CAS  Google Scholar 

  • Maseda H, Hoshino T (1995) Screening and analysis of DNA fragments that show promoter activities in Thermus thermophilus. FEMS Microbiol Lett 128:127–134

    PubMed  CAS  Google Scholar 

  • Masui R, Kurokawa K, Nakagawa N, Tokunaga F, Koyama Y, Shibata T, Oshima T, Yokoyama S, Yasunaga T, Kuramitsu S, NCBI (2005) Thermus thermophilus HB8, complete genome. http://www.ncbi.nlm.nih.gov/sites/entrez?db=genome&cmd=Retrieve&dopt=Overview&list_uids=530

  • Mather MW, Fee JA (1992) Development of plasmid cloning vectors for Thermus thermophilus HB8: expression of a heterologous, plasmid-borne kanamycin nucleotidyltransferase gene. Appl Environ Microbiol 58:421–425

    PubMed  CAS  Google Scholar 

  • Matsumi R, Manabe K, Fukui T, Atomi H, Imanaka T (2007) Disruption of a sugar transporter gene cluster in a hyperthermophilic archaeon using a host-marker system based on antibiotic resistance. J Bacteriol 189:2683–2691

    PubMed  CAS  Google Scholar 

  • Matsumura M, Aiba S (1985) Screening for thermostable mutant of kanamycin nucleotidyltransferase by the use of a transformation system for a thermophile, Bacillus stearothermophilus. J Biol Chem 260:15298–15303

    PubMed  CAS  Google Scholar 

  • Matsumura M, Katakura Y, Imanaka T, Aiba S (1984) Enzymatic and nucleotide sequence studies of a kanamycin-inactivating enzyme encoded by a plasmid from thermophilic bacilli in comparison with that encoded by plasmid pUB110. J Bacteriol 160:413–420

    PubMed  CAS  Google Scholar 

  • Mesbah NM, Hedrick DB, Peacock AD, Rohde M, Wiegel J (2007) Natranaerobius thermophilus gen. nov., sp. nov., a halophilic, alkalithermophilic bacterium from soda lakes of the Wadi An Natrun, Egypt, and proposal of Natranaerobiaceae fam. nov. and Natranaerobiales ord. nov. Int J Syst Evol Microbiol 57:2507–2512

    PubMed  CAS  Google Scholar 

  • Minakhin L, Goel M, Berdygulova Z, Ramanculov E, Florens L, Glazko G, Karamychev VN, Slesarev AI, Kozyavkin SA, Khromov I, Ackermann HW, Washburn M, Mushegian A, Severinov K (2008) Genome comparison and proteomic characterization of Thermus thermophilus bacteriophages P23-45 and P74-26: siphoviruses with triplex-forming sequences and the longest known tails. J Mol Biol 378:468–480

    PubMed  CAS  Google Scholar 

  • Mooser D, Maneg O, Corvey C, Steiner T, Malatesta F, Karas M, Soulimane T, Ludwig B (2005) A four-subunit cytochrome bc(1) complex complements the respiratory chain of Thermus thermophilus. Biochim Biophys Acta 1708:262–274

    PubMed  CAS  Google Scholar 

  • Mooser D, Maneg O, MacMillan F, Malatesta F, Soulimane T, Ludwig B (2006) The menaquinol-oxidizing cytochrome bc complex from Thermus thermophilus: protein domains and subunits. Biochim Biophys Acta 1757:1084–1095

    PubMed  CAS  Google Scholar 

  • Moreno R, Zafra O, Cava F, Berenguer J (2003) Development of a gene expression vector for Thermus thermophilus based on the promoter of the respiratory nitrate reductase. Plasmid 49:2–8

    PubMed  CAS  Google Scholar 

  • Moreno R, Haro A, Castellanos A, Berenguer J (2005) High-level overproduction of His-tagged Tth DNA polymerase in Thermus thermophilus. Appl Environ Microbiol 71:591–593

    PubMed  CAS  Google Scholar 

  • Müller V, Gruber G (2003) ATP synthases: structure, function and evolution of unique energy converters. Cell Mol Life Sci 60:474–494

    PubMed  Google Scholar 

  • Munster MJ, Munster AP, Sharp RJ (1985) Incidence of Plasmids in Thermus spp. Isolated in Yellowstone National Park. Appl Environ Microbiol 50:1325–1327

    PubMed  CAS  Google Scholar 

  • Muresanu L, Pristovsek P, Lohr F, Maneg O, Mukrasch MD, Ruterjans H, Ludwig B, Lucke C (2006) The electron transfer complex between cytochrome c552 and the CuA domain of the Thermus thermophilus ba3 oxidase: a combined NMR and computational approach. J Biol Chem 281:14503–14513

    PubMed  CAS  Google Scholar 

  • Nakamura A, Takakura Y, Kobayashi H, Hoshino T (2005) In vivo directed evolution for thermostabilization of Escherichia coli hygromycin B phosphotransferase and the use of the gene as a selection marker in the host-vector system of Thermus thermophilus. J Biosci Bioeng 100:158–163

    PubMed  CAS  Google Scholar 

  • Naryshkina T, Liu J, Florens L, Swanson SK, Pavlov AR, Pavlova NV, Inman R, Minakhin L, Kozyavkin SA, Washburn M, Mushegian A, Severinov K (2006) Thermus thermophilus bacteriophage phiYS40 genome and proteomic characterization of virions. J Mol Biol 364:667–677

    PubMed  CAS  Google Scholar 

  • Nesper J, Brosig A, Ringler P, Patel GJ, Muller SA, Kleinschmidt JH, Boos W, Diederichs K, Welte W (2008) TtOmp85 from Thermus thermophilus HB27: an ancestral type of the Omp85 protein family. J Bacteriol 190:4568–4575

  • Nunes OC, Manaia CM, Da Costa MS, Santos H (1995) Compatible Solutes in the Thermophilic Bacteria Rhodothermus marinus and “Thermus thermophilus”. Appl Environ Microbiol 61:2351–2357

    PubMed  CAS  Google Scholar 

  • Ohta T, Tokishita S, Imazuka R, Mori I, Okamura J, Yamagata H (2006) beta-Glucosidase as a reporter for the gene expression studies in Thermus thermophilus and constitutive expression of DNA repair genes. Mutagenesis 21:255–260

    PubMed  CAS  Google Scholar 

  • Olabarría G, Fernandez-Herrero LA, Carrascosa JL, Berenguer J (1996) slpM, a gene coding for an “S-layer-like array” overexpressed in S- layer mutants of Thermus thermophilus HB8. J Bacteriol 178:357–365

    PubMed  Google Scholar 

  • Omelchenko MV, Wolf YI, Gaidamakova EK, Matrosova VI, Vasilenko A, Zhai M, Daly MJ, Koonin EV, Makarova KS (2005) Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: divergent routes of adaptation to thermophily and radiation resistance. BMC Evolut Biol 5:57

    Google Scholar 

  • Oshima T (2007) Unique polyamines produced by an extreme thermophile, Thermus thermophilus. Amino Acids 33:367–372

    PubMed  CAS  Google Scholar 

  • Pai RD, Zhang W, Schuwirth BS, Hirokawa G, Kaji H, Kaji A, Cate JH (2008) Structural Insights into ribosome recycling factor interactions with the 70S ribosome. J Mol Biol 376:1334–1347

    PubMed  CAS  Google Scholar 

  • Pantazaki AA, Pritsa AA, Kyriakidis DA (2002) Biotechnologically relevant enzymes from Thermus thermophilus. Appl Microbiol Biotechnol 58:1–12

    PubMed  CAS  Google Scholar 

  • Park HJ, Reiser CO, Kondruweit S, Erdmann H, Schmid RD, Sprinzl M (1992) Purification and characterization of a NADH oxidase from the thermophile Thermus thermophilus HB8. Eur J Biochem 205:881–885

    PubMed  CAS  Google Scholar 

  • Park T, Lee J-H, Kim H-K, Hoe H-S, Kwon S-T (1999) Nucleotide sequence of the gene for alkaline phosphatase of Thermus caldophilus GK24 and characteristics of the deduced primary structure of the enzyme. FEMS Microbiol Lett 180:133–139

    PubMed  CAS  Google Scholar 

  • Park HS, Kayser KJ, Kwak JH, Kilbane JJ 2nd (2004) Heterologous gene expression in Thermus thermophilus: beta-galactosidase, dibenzothiophene monooxygenase, PNB carboxy esterase, 2-aminobiphenyl-2, 3-diol dioxygenase, and chloramphenicol acetyl transferase. J Ind Microbiol Biotechnol 31:189–197

    Article  PubMed  CAS  Google Scholar 

  • Park SH, Kang HK, Shim JH, Woo EJ, Hong JS, Kim JW, Oh BH, Lee BH, Cha H, Park KH (2007) Modulation of substrate preference of Thermus maltogenic amylase by mutation of the residues at the interface of a dimer. Biosci Biotechnol Biochem 71:1564–1567

    PubMed  CAS  Google Scholar 

  • Pask-Hughes RA, Shaw N (1982) Glycolipids from some extreme thermophilic bacteria belonging to the genus Thermus. J Bacteriol 149:54–58

    PubMed  CAS  Google Scholar 

  • Pedelacq JD, Cabantous S, Tran T, Terwilliger TC, Waldo GS (2006) Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol 24:79–88

    PubMed  CAS  Google Scholar 

  • Pederson DM, Welsh LC, Marvin DA, Sampson M, Perham RN, Yu M, Slater MR (2001) The protein capsid of filamentous bacteriophage PH75 from Thermus thermophilus. J Mol Biol 309:401–421

    PubMed  CAS  Google Scholar 

  • Perales C, Cava F, Meijer W, Berenguer J (2003) Enhancement of DNA, cDNA synthesis and fidelity at high temperatures by a dimeric single-stranded DNA-binding protein. Nucleic Acids Res 31:6473–6480

    PubMed  CAS  Google Scholar 

  • Pessela BCC, Vian A, Guisán JM, Carrascosa AV, Fernández-Lafuente R, Mateo C, García JL (2003) Hydrolysis of lactose with immobilised thermoresistant lactase and the production method thereof. Spain. Patent number WO03070928

  • Pessela BCC, Fernandez-Lafuente R, Torres R, Mateo C, Fuentes M, Filho M, Vian A, Garcia JL, Guisan JM, Carrascosa AV (2007) Production of a thermoresistant alpha-galactosidase from Thermus sp strain T2 for food processing. Food Biotechnol 21:91–103

    CAS  Google Scholar 

  • Philippot L (2002) Denitrifying genes in Bacterial and Archaeal genomes. Biochim Biophys Acta 1577:355–376

    PubMed  CAS  Google Scholar 

  • Prescott M, Battad JM, Wilmann PG, Rossjohn J, Devenish RJ (2006) Recent advances in all-protein chromophore technology. Biotechnol Annu Rev 12:31–66

    PubMed  CAS  Google Scholar 

  • Quintela JC, Pittenauer E, Allmaier G, Aran V, de Pedro MA (1995) Structure of peptidoglycan from Thermus thermophilus HB8. J Bacteriol 177:4947–4962

    PubMed  CAS  Google Scholar 

  • Quintela JC, Garcia-del Portillo F, Pittenauer E, Allmaier G, de Pedro MA (1999) Peptidoglycan fine structure of the radiotolerant bacterium Deinococcus radiodurans Sark. J Bacteriol 181:334–337

    PubMed  CAS  Google Scholar 

  • Radax C, Sigurdsson O, Hreggvidsson GO, Aichinger N, Gruber C, Kristjansson JK, Stan-Lotter H (1998) F-and V-ATPases in the genus Thermus and related species. Syst Appl Microbiol 21:12–22

    PubMed  CAS  Google Scholar 

  • Ramírez-Arcos S, Fernandez-Herrero LA, Marin I, Berenguer J (1998) Anaerobic growth, a property horizontally transferred by an Hfr-like mechanism among extreme thermophiles. J Bacteriol 180:3137–3143

    PubMed  Google Scholar 

  • Ramïrez-Arcos S, Moreno R, Zafra O, Castan P, Valles C, Berenguer J (2000) Two nitrate/nitrite transporters are encoded within the mobilizable plasmid for nitrate respiration of Thermus thermophilus HB8. J Bacteriol 182:2179–2183

    Google Scholar 

  • Ruan L, Xu X (2007) Sequence analysis and characterizations of two novel plasmids isolated from Thermus sp. 4C. Plasmid 58:84–87

    PubMed  CAS  Google Scholar 

  • Rumszauer J, Schwarzenlander C, Averhoff B (2006) Identification, subcellular localization and functional interactions of PilMNOWQ and PilA4 involved in transformation competency and pilus biogenesis in the thermophilic bacterium Thermus thermophilus HB27. FEBS J 273:3261–3272

    PubMed  CAS  Google Scholar 

  • Sakaki Y, Oshima T (1975) Isolation and characterization of a bacteriophage infectious to an extreme thermophile, Thermus thermophilus HB8. J Virol 15:1449–1453

    PubMed  CAS  Google Scholar 

  • Sato T, Fukui T, Atomi H, Imanaka T (2003) Targeted gene disruption by homologous recombination in the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J Bacteriol 185:210–220

    PubMed  CAS  Google Scholar 

  • Sato T, Fukui T, Atomi H, Imanaka T (2005) Improved and versatile transformation system allowing multiple genetic manipulations of the hyperthermophilic archaeon Thermococcus kodakaraensis. Appl Environ Microbiol 71:3889–3899

    PubMed  CAS  Google Scholar 

  • Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430–1436

    PubMed  CAS  Google Scholar 

  • Schwarzenlander C, Averhoff B (2006) Characterization of DNA transport in the thermophilic bacterium Thermus thermophilus HB27. FEBS J 273:4210–4218

    PubMed  CAS  Google Scholar 

  • Selmer M, Dunham CM, Murphy FVT, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935–1942

    PubMed  CAS  Google Scholar 

  • Severinov K (2000) RNA polymerase structure-function: insights into points of transcriptional regulation. Curr Opin Microbiol 3:118–125

    PubMed  CAS  Google Scholar 

  • Sevostyanova A, Djordjevic M, Kuznedelov K, Naryshkina T, Gelfand MS, Severinov K, Minakhin L (2007) Temporal regulation of viral transcription during development of Thermus thermophilus bacteriophage phiYS40. J Mol Biol 366:420–435

    PubMed  CAS  Google Scholar 

  • Shigemori Y, Oishi M (2004) Specific cleavage of DNA molecules at RecA-mediated triple-strand structure. Nucleic Acids Res 32:e4

    PubMed  Google Scholar 

  • Shigemori Y, Oishi M (2005) Stable triple-stranded DNA formation and its application to the SNP detection. DNA Res 12:441–449

    PubMed  CAS  Google Scholar 

  • Smile DH, Donohue M, Yeh MF, Kenkel T, Trela JM (1977) Repressible alkaline phosphatase from Thermus aquaticus: associated phosphodiesterase activity. J Biol Chem 252:3399–3401

    PubMed  CAS  Google Scholar 

  • Soulimane T, Buse G, Bourenkov GP, Bartunik HD, Huber R, Than ME (2000) Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from Thermus thermophilus. EMBO J 19:1766–1776

    PubMed  CAS  Google Scholar 

  • Stupak M, Zoldak G, Musatov A, Sprinzl M, Sedlak E (2006) Unusual effect of salts on the homodimeric structure of NADH oxidase from Thermus thermophilus in acidic pH. Biochim Biophys Acta 1764:129–137

    PubMed  CAS  Google Scholar 

  • Szybalski W (1997) RecA-mediated Achilles’ heel cleavage. Curr Opin Biotechnol 8:75–81

    PubMed  CAS  Google Scholar 

  • Takahashi M, Yamaguchi E, Uchida T (1984) Thermophilic DNA ligase: purification and properties of the enzyme from Thermus thermophilus HB8. J Biol Chem 259:10041–10047

    PubMed  CAS  Google Scholar 

  • Takayama G, Kosuge T, Maseda H, Nakamura A, Hoshino T (2004) Nucleotide sequence of the cryptic plasmid pTT8 from Thermus thermophilus HB8 and isolation and characterization of its high-copy-number mutant. Plasmid 51:227–237

    PubMed  CAS  Google Scholar 

  • Tamakoshi M, Yamagishi A, Oshima T (1995) Screening of stable proteins in an extreme thermophile, Thermus thermophilus. Mol Microbiol 16:1031–1036

    PubMed  CAS  Google Scholar 

  • Tamakoshi M, Uchida M, Tanabe K, Fukuyama S, Yamagishi A, Oshima T (1997) A new Thermus-Escherichia coli shuttle integration vector system. J Bacteriol 179:4811–4814

    PubMed  CAS  Google Scholar 

  • Tamakoshi M, Yaoi T, Oshima T, Yamagishi A (1999) An efficient gene replacement and deletion system for an extreme thermophile, Thermus thermophilus. FEMS Microbiol Lett 173:431–437

    PubMed  CAS  Google Scholar 

  • Tamakoshi M, Nakano Y, Kakizawa S, Yamagishi A, Oshima T (2001) Selection of stabilized 3-isopropylmalate dehydrogenase of Saccharomyces cerevisiae using the host-vector system of an extreme thermophile, Thermus thermophilus. Extremophiles 5:17–22

    PubMed  CAS  Google Scholar 

  • Terui Y, Ohnuma M, Hiraga K, Kawashima E, Oshima T (2005) Stabilization of nucleic acids by unusual polyamines produced by an extreme thermophile, Thermus thermophilus. Biochem J 388:427–433

    PubMed  CAS  Google Scholar 

  • Teshima T, Kohda J, Kondo A, Taguchi H, Yohda M, Endo I, Fukuda H (1998) Protein refolding system using holo-chaperonin from the thermophilic bacterium Thermus thermophilus. J Ferment Bioeng 85:564–570

    CAS  Google Scholar 

  • Toei M, Gerle C, Nakano M, Tani K, Gyobu N, Tamakoshi M, Sone N, Yoshida M, Fujiyoshi Y, Mitsuoka K, Yokoyama K (2007) Dodecamer rotor ring defines H+/ATP ratio for ATP synthesis of prokaryotic V-ATPase from Thermus thermophilus. Proc Natl Acad Sci USA 104:20256–20261

    PubMed  CAS  Google Scholar 

  • Tong J, Cao W, Barany F (1999) Biochemical properties of a high fidelity DNA ligase from Thermus species AK16D. Nucleic Acids Res 27:788–794

    PubMed  CAS  Google Scholar 

  • Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65:1–43

    PubMed  CAS  Google Scholar 

  • Watrin L, Lucas S, Purcarea C, Legrain C, Prieur D (1999) Isolation and characterization of pyrimidine auxotrophs, and molecular cloning of the pyrE gene from the hyperthermophilic archaeon Pyrococcus abyssi. Mol Gen Genet 262:378–381

    PubMed  CAS  Google Scholar 

  • Wayne J, Xu SY (1997) Identification of a thermophilic plasmid origin and its cloning within a new Thermus-E. coli shuttle vector. Gene 195:321–328

    PubMed  CAS  Google Scholar 

  • Weisburg WG, Giovannoni SJ, Woese CR (1989) The Deinococcus-Thermus phylum and the effect of rRNA composition on phylogenetic tree construction. Syst Appl Microbiol 11:128–134

    PubMed  CAS  Google Scholar 

  • Witzmann S, Bisswanger H (1998) The pyruvate dehydrogenase complex from thermophilic organisms: thermal stability and re-association from the enzyme components. Biochim Biophys Acta 1385:341–352

    PubMed  CAS  Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    PubMed  CAS  Google Scholar 

  • Worthington P, Hoang V, Perez-Pomares F, Blum P (2003) Targeted disruption of the alpha-amylase gene in the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 185:482–488

    PubMed  CAS  Google Scholar 

  • Yagi T, Hon-nami K, Ohnishi T (1988) Purification and characterization of two types of NADH-quinone reductase from Thermus thermophilus HB-8. Biochemistry 27:2008–2013

    PubMed  CAS  Google Scholar 

  • Yano T, Chu SS, Sled VD, Ohnishi T, Yagi T (1997) The proton-translocating NADH-quinone oxidoreductase (NDH-1) of thermophilic bacterium Thermus thermophilus HB-8: complete DNA sequence of the gene cluster and thermostable properties of the expressed NQO2 subunit. J Biol Chem 272:4201–4211

    PubMed  CAS  Google Scholar 

  • Yokoyama K, Akabane Y, Ishii N, Yoshida M (1994) Isolation of prokaryotic V0V1-ATPase from a thermophilic eubacterium Thermus thermophilus. J Biol Chem 269:12248–12253

    PubMed  CAS  Google Scholar 

  • Yokoyama K, Ohkuma S, Taguchi H, Yasunaga T, Wakabayashi T, Yoshida M (2000a) V-Type H+-ATPase/synthase from a thermophilic eubacterium, Thermus thermophilus: subunit structure and operon. J Biol Chem 275:13955–13961

    PubMed  CAS  Google Scholar 

  • Yokoyama S, Hirota H, Kigawa T, Yabuki T, Shirouzu M, Terada T, Ito Y, Matsuo Y, Kuroda Y, Nishimura Y, Kyogoku Y, Miki K, Masui R, Kuramitsu S (2000b) Structural genomics projects in Japan. Nat Struct Biol 7(Suppl):943–945

    PubMed  CAS  Google Scholar 

  • Yu JS, Noll KM (1997) Plasmid pRQ7 from the hyperthermophilic bacterium Thermotoga species strain RQ7 replicates by the rolling-circle mechanism. J Bacteriol 179:7161–7164

    PubMed  CAS  Google Scholar 

  • Yu JS, Vargas M, Mityas C, Noll KM (2001) Liposome-mediated DNA uptake and transient expression in Thermotoga. Extremophiles 5:53–60

    PubMed  CAS  Google Scholar 

  • Yu MX, Slater MR, Ackermann HW (2006) Isolation and characterization of Thermus bacteriophages. Arch Virol 151:663–679

    PubMed  CAS  Google Scholar 

  • Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF (2001) Crystal structure of the ribosome at 5.5 A resolution. Science 292:883–896

    PubMed  CAS  Google Scholar 

  • Yusupova GZ, Yusupov MM, Cate JH, Noller HF (2001) The path of messenger RNA through the ribosome. Cell 106:233–241

    PubMed  CAS  Google Scholar 

  • Zafra O, Ramírez S, Castán P, Moreno R, Cava F, Valles C, Caro E, Berenguer J (2002) A cytochrome c encoded by the nar operon is required for the synthesis of active respiratory nitrate reductase in Thermus thermophilus. FEBS Lett 523:99–102

    PubMed  CAS  Google Scholar 

  • Zafra O, Cava F, Blasco F, Magalon A, Berenguer J (2005) Membrane-associated maturation of the heterotetrameric nitrate reductase of Thermus thermophilus. J Bacteriol 187:3990–3996

    PubMed  CAS  Google Scholar 

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Rev 61(4):533–616

    CAS  Google Scholar 

Download references

Acknowledgments

This work has been supported by grants of code BIO2007-60245 and S0505/PPQ/0344 from the “Ministerio de Educación y Ciencia” and the “Comunidad Autónoma de Madrid”, respectively. A. Hidalgo is supported by a “Ramón y Cajal “contract. An institutional grant from Fundación Ramón Areces to CBMSO is also acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Berenguer.

Additional information

Communicated by T. Matsunaga.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cava, F., Hidalgo, A. & Berenguer, J. Thermus thermophilus as biological model. Extremophiles 13, 213–231 (2009). https://doi.org/10.1007/s00792-009-0226-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-009-0226-6

Keywords

Navigation