Applied Microbiology and Biotechnology

, Volume 102, Issue 24, pp 10425–10437 | Cite as

Peculiarities and biotechnological potential of environmental adaptation by Geobacillus species

  • Hirokazu SuzukiEmail author


The genus Geobacillus comprises thermophilic bacilli capable of endospore formation. The members of this genus provide thermostable proteins and can be used in whole cell applications at elevated temperatures; therefore, these organisms are of biotechnological importance. While these applications have been described in previous reviews, the present paper highlights the environmental adaptations and genome diversifications of Geobacillus spp. and their applications in evolutionary-protein engineering. Despite their obligate thermophilic properties, Geobacillus spp. are widely distributed in nature. Because several isolates demonstrate remarkable properties for cell reproduction in their respective niches, they seem to exist not only as endospores but also as vegetative cells in diverse environments. This suggests their excellence in environmental adaptation via genome diversification; in fact, evidence suggests that Geobacillus spp. were derived from Bacillus spp. while diversifying their genomes via horizontal gene transfer. Moreover, when subjected to an environmental stressor, Geobacillus spp. diversify their genomes using inductive mutations and transposable elements to produce derivative cells that are adaptive to the stressor. Notably, inductive mutations in Geobacillus spp. occur more rapidly and frequently than the stress-induced mutagenesis observed in other microorganisms. Owing to this, Geobacillus spp. can efficiently generate mutant genes coding for thermostable enzyme variants from the thermolabile enzyme genes under appropriate selection pressures. This phenomenon provides a new approach to generate thermostable enzymes, termed as thermoadaptation-directed enzyme evolution, thereby expanding the biotechnological potentials of Geobacillus spp. In this review, we have discussed this approach using successful examples and major challenges yet to be addressed.


Environmental adaptation Geobacillus Genome diversification Thermophile Thermostable enzymes 


Funding information

This work was funded by the following organizations: Japan Society for the Promotion of Science (Grant numbers: 25450105 and 17K06925); Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry, Japan; the Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry, Japan; Nagase Science and Technology Foundation; and the Institute for Fermentation, Osaka, Japan.

Compliance with ethical standards

Conflict of interest

The author declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by the author.


  1. Abd Rahman RNZR, Leow TC, Salleh AB, Basri M (2007) Geobacillus zalihae sp. nov., a thermophilic lipolytic bacterium isolated from palm oil mill effluent in Malaysia. BMC Microbiol 7:77. CrossRefPubMedGoogle Scholar
  2. Aliyu H, Lebre P, Blom J, Cowan D, De Maayer P (2016) Phylogenomic re-assessment of the thermophilic genus Geobacillus. Syst Appl Microbiol 39:527–533.; erratum to this report can be found in
  3. Alkhalili RN, Hatti-Kaul R, Canbäck B (2015) Genome sequence of Geobacillus sp. strain ZGt-1, an antibacterial peptide-producing bacterium from hot springs in Jordan. Genome Announc 3:e00799–15. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Amoozegar MA, Bagheri M, Makhdoumi A, Mehrshad M, Didari M, Schumann P, Spröer C, Sánchez-Porro C, Ventosa A (2016) Oceanobacillus longus sp. nov., a moderately halophilic bacterium isolated from a salt lake. Int J Syst Evol Microbiol 66:4225–4230.
  5. Anutrakunchai C, Niamsanit S, Wangsomnuk PP, Trongpanich Y (2010) Isolation and characterization of vitamin B6-producing thermophilic bacterium, Geobacillus sp. H6a. J Gen Appl Microbiol 56:273–279. CrossRefPubMedGoogle Scholar
  6. Ash C, Farrow JAE, Wallbanks S, Collins MD (1991) Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small-subunit-ribosomal RNA sequences. Lett Appl Microbiol 13:202–206. CrossRefGoogle Scholar
  7. Asial I, Cheng YX, Engman H, Dollhopf M, Wu B, Nordlund P, Cornvik T (2013) Engineering protein thermostability using a generic activity-independent biophysical screen inside the cell. Nat Commun 4:2901.
  8. Assareh R, Zahiri HS, Noghabi KA, Aminzadeh S, Khaniki GB (2012) Characterization of the newly isolated Geobacillus sp. T1, the efficient cellulase-producer on untreated barley and wheat straws. Bioresour Technol 120:99–105. CrossRefPubMedGoogle Scholar
  9. Banat IM, Marchant R, Rahman TJ (2004) Geobacillus debilis sp. nov., a novel obligately thermophilic bacterium isolated from a cool soil environment, and reassignment of Bacillus pallidus to Geobacillus pallidus comb. nov. Int J Syst Evol Microbiol 54:2197–2201. CrossRefPubMedGoogle Scholar
  10. Bartholomew JW, Paik G (1966) Isolation and identification of obligate thermophilic sporeforming bacilli from ocean basin cores. J Bacteriol 92:635–638PubMedPubMedCentralGoogle Scholar
  11. Bergdale TE, Hughes SR, Bang SS (2014) Thermostable hemicellulases of a bacterium, Geobacillus sp. DC3, isolated from the former Homestake gold mine in Lead, South Dakota. Appl Biochem Biotechnol 172:3488–3501. CrossRefPubMedGoogle Scholar
  12. Bezuidt OK, Pierneef R, Gomri AM, Adesioye F, Makhalanyane TP, Kharroub K, Cowan DA (2016) The Geobacillus pan-genome: implications for the evolution of the genus. Front Microbiol 7:723. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bhalla A, Kainth AS, Sani RK (2013) Draft genome sequence of lignocellulose-degrading thermophilic bacterium Geobacillus sp. strain WSUCF1. Genome Announc 1:e00595–13. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bommarius AS, Broering JM, Chaparro-Riggers JF, Polizzi KM (2006) High-throughput screening for enhanced protein stability. Curr Opin Biotechnol 17:606–610. CrossRefGoogle Scholar
  15. Bose S, Mukherjee T, Sen U, Roy C, Rameez MJ, Ghosh W, Mukhopadhyay SK (2016) Genome sequence of the multiple-protease-producing strain Geobacillus thermoleovorans N7, a thermophilic bacterium isolated from Paniphala Hot Spring, West Bengal, India. Genome Announc 4:e01202–16. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bosma EF, van de Weijer AHP, Daas MJA, van der Oost J, de Vos WM, van Kranenburg R (2015) Isolation and screening of thermophilic bacilli from compost for electrotransformation and fermentation: characterization of Bacillus smithii ET 138 as a new biocatalyst. Appl Environ Microbiol 81:1874–1883. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Brouns SJJ, 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. CrossRefPubMedGoogle Scholar
  18. Brumm P, Land ML, Hauser LJ, Jeffries CD, Chang Y, Mead DA (2015a) Complete genome sequences of Geobacillus sp. Y412MC52, a xylan-degrading strain isolated from obsidian hot spring in Yellowstone National Park. Stand Genomic Sci 10:81.; erratum to this report can be found in
  19. Brumm PJ, Land ML, Mead DA (2015b) Complete genome sequence of Geobacillus thermoglucosidasius C56-YS93, a novel biomass degrader isolated from obsidian hot spring in Yellowstone National Park. Stand Genomic Sci 10:73.
  20. Brumm PJ, Land ML, Mead DA (2016) Complete genome sequences of Geobacillus sp. WCH70, a thermophilic strain isolated from wood compost. Stand Genomic Sci 11:33. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Bryanskaya AV, Rozanov AS, Logacheva MD, Kotenko AV, Peltek SE (2014) Draft genome sequence of Geobacillus icigianus strain G1w1T isolated from hot springs in the valley of Geysers, Kamchatka (Russian Federation). Genome Announc 2:e01098–14. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Burgess SA, Flint SH, Lindsay D (2013) Characterization of thermophilic bacilli from a milk powder processing plant. J Appl Microbiol 116:350–359. CrossRefPubMedGoogle Scholar
  23. Burgess SA, Flint SH, Lindsay D, Cox MP, Biggs PJ (2017) Insights into the Geobacillus stearothermophilus species based on phylogenomic principles. BMC Microbiol 17:140.
  24. Carlson C, Singh NK, Bibra M, Sani RK, Venkateswaran K (2018) Pervasiveness of UVC254-resistant Geobacillus strains in extreme environments. Appl Microbiol Biotechnol 102:1869–1887. CrossRefPubMedGoogle Scholar
  25. Chamkha M, Mnif S, Sayadi S (2008) Isolation of a thermophilic and halophilic tyrosol-degrading Geobacillus from a Tunisian high-temperature oil field. FEMS Microbiol Lett 283:23–29. CrossRefPubMedGoogle Scholar
  26. Charbonneau DM, Meddeb-Mouelhi F, Boissinot M, Sirois M, Beauregard M (2012) Identification of thermophilic bacterial strains producing thermotolerant hydrolytic enzymes from manure compost. Indian J Microbiol 52:41–47. CrossRefPubMedGoogle Scholar
  27. 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. CrossRefPubMedGoogle Scholar
  28. Coorevits A, Dinsdale AE, Halket G, Lebbe L, De Vos P, Van Landschoot A, Logan NA (2012) Taxonomic revision of the genus Geobacillus: emendation of Geobacillus, G. stearothermophilus, G. jurassicus, G. toebii, G. thermodenitrificans and G. thermoglucosidans (nom. corrig., formerly ‘thermoglucosidasius’); transfer of Bacillus thermantarcticus to the genus as G. thermantarcticus comb. nov.; proposal of Caldibacillus debilis gen. nov., comb. nov.; transfer of G. tepidamans to Anoxybacillus as A. tepidamans comb. nov.; and proposal of Anoxybacillus caldiproteolyticus sp. nov. Int J Syst Evol Microbiol 62:1470–1485. CrossRefPubMedGoogle Scholar
  29. Correa-Llantén D, Larraín-Linton J, Muñoz PA, Castro M, Boehmwald F, Blamey JM (2013) Characterization of the thermophilic bacterium Geobacillus sp. strain GWE1 isolated from a sterilization oven. J Microbiol Biotechnol 41:278–283. CrossRefGoogle Scholar
  30. Cuebas M, Sannino D, Bini E (2011) Isolation and characterization of an arsenic resistant Geobacillus kaustophilus strain from geothermal soils. J Basic Microbiol 51:364–371. CrossRefPubMedGoogle Scholar
  31. Daas MJA, Vriesendorp B, van de Weijer AHP, van der Oost J, van Kranenburg R (2018) Complete genome sequence of Geobacillus thermodenitrificans T12, a potential host for biotechnological applications. Curr Microbiol 75:49–56. CrossRefPubMedGoogle Scholar
  32. Daroonpunt R, Tanasupawat S, Kudo T, Ohkuma M, Itoh T (2016) Virgibacillus kapii sp. nov., isolated from Thai shrimp paste (Ka-pi). Int J Syst Evol Microbiol 66:1832–1837. CrossRefPubMedGoogle Scholar
  33. Das S, Jean J, Kar S, Chou M, Chen C (2014) Screening of plant growth-promoting traits in arsenic-resistant bacteria isolated from agricultural soil and their potential implication for arsenic bioremediation. J Hazard Mater 272:112–120. CrossRefPubMedGoogle Scholar
  34. De Maayer P, Brumm PJ, Mead DA, Cowan DA (2014) Comparative analysis of the Geobacillus hemicellulose utilization locus reveals a highly variable target for improved hemicellulolysis. BMC Genomics 15:836. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Di Donato P, Romano I, Mastascusa V, Poli A, Orlando P, Pugliese M, Nicolaus B (2018) Survival and adaptation of the thermophilic species Geobacillus thermantarcticus in simulated spatial conditions. Orig Life Evol Biosph 48:141–158. CrossRefPubMedGoogle Scholar
  36. Didari M, Amoozegar MA, Bagheri M, Schumann P, Spröer C, Sánchez-Porro C, Ventosa A (2012) Alteribacillus bidgolensis gen. nov., sp. nov., a moderately halophilic bacterium from a hypersaline lake, and reclassification of Bacillus persepolensis as Alteribacillus persepolensis comb. nov. Int J Syst Evol Microbiol 62:2691–2697. CrossRefPubMedGoogle Scholar
  37. Donk PJ (1920) A highly resistant thermophilic organism. J Bacteriol 5:373–374PubMedPubMedCentralGoogle Scholar
  38. Drejer EB, Hakvåg S, Irla M, Brautaset T (2018) Genetic tools and techniques for recombinant expression in thermophilic Bacillaceae. Microorganisms 6:E42. CrossRefPubMedGoogle Scholar
  39. Egan K, Kelleher P, Field D, Rea MC, Ross RP, Cotter PD, Hill C (2017) Genome sequence of Geobacillus stearothermophilus DSM 458, an antimicrobial-producing thermophilic bacterium, isolated from a sugar beet factory. Genome Announc 5:e01172–17. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Feng L, Wang W, Cheng J, Ren Y, Zhao G, Gao C, Tang Y, Liu X, Han W, Peng X, Liu R, Wang L (2007) Genome and proteome of long-chain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir. Proc Natl Acad Sci U S A 104:5602–5607. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Fields ML, Chen Lee PP (1974) Bacillus stearothermophilus in soils of Iceland. Appl Microbiol 28:638–640PubMedPubMedCentralGoogle Scholar
  42. Foit L, Morgan GJ, Kern MJ, Steimer LR, von Hacht AA, Titchmarsh J, Warriner SL, Radford SE, Bardwell JCA (2009) Optimizing protein stability in vivo. Mol Cell 36:861–871. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Foster PL (2007) Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol 42:373–397. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Frenzel E, Legebeke J, van Stralen A, van Kranenburg R, Kuipers OP (2018) In vivo selection of sfGFP variants with improved and reliable functionality in industrially important thermophilic bacteria. Biotechnol Biofuels 11:8. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Fujii K, Tominaga Y, Okunaka J, Yagi H, Ohshiro T, Suzuki H (2018) Microbial and genomic characterization of Geobacillus thermodenitrificans OS27, a marine thermophile that degrades diverse raw seaweeds. Appl Microbiol Biotechnol 102:4901–4913. CrossRefPubMedGoogle Scholar
  46. Gaultier NE, Junqueira ACM, Uchida A, Purbojati RW, Houghton JNI, Chénard C, Wong A, Kolundžija S, Clare ME, Kushwaha KK, Panicker D, Putra A, Kee C, Premkrishnan BNV, Heinle CE, Lim SBY, Vettath VK, Drautz-Moses DI, Schuster SC (2018) Genome sequence of Geobacillus thermoleovorans SGAir0734, isolated from Singapore air. Genome Announc 6:e00636–18.
  47. Goh KM, Kahar UM, Chai YY, Chong CS, Chai KP, Ranjani V, Illias RM, Chan K (2013) Recent discoveries and applications of Anoxybacillus. Appl Microbiol Biotechnol 97:1475–1488. CrossRefPubMedGoogle Scholar
  48. Gordon RE, Smith NR (1949) Aerobic sporeforming bacteria capable of growth at high temperatures. J Bacteriol 56:327–341Google Scholar
  49. Harrington LB, Paez-Espino D, Staahl BT, Chen JS, Ma E, Kyrpides NC, Doudna JA (2017) A thermostable Cas9 with increased lifetime in human plasma. Nat Commun 8:1424. CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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. CrossRefPubMedGoogle Scholar
  51. Hussein AH, Lisowska BK, Leak DJ (2015) The genus Geobacillus and their biotechnological potential. Adv Appl Microbiol 92:1–48. CrossRefPubMedGoogle Scholar
  52. Imanaka T, Fujii M, Aramori I, Aiba S (1982) Transformation of Bacillus stearothermophilus with plasmid DNA and characterization of shuttle vector plasmids between Bacillus stearothermophilus and Bacillus subtilis. J Bacteriol 149:824–830PubMedPubMedCentralGoogle Scholar
  53. Jeon CO, Lim J, Lee J, Xu L, Jiang C, Kim C (2005) Reclassification of Bacillus haloalkaliphilus Fritze 1996 as Alkalibacillus haloalkaliphilus gen. nov., comb. nov. and the description of Alkalibacillus salilacus sp. nov., a novel halophilic bacterium isolated from a salt lake in China. Int J Syst Evol Microbiol 55:1891–1896. CrossRefPubMedGoogle Scholar
  54. Juárez AGV, Dreyer J, Göpel PK, Koschke N, Frank D, Märkl H, Müller R (2009) Characterisation of a new thermoalkaliphilic bacterium for the production of high-quality hemp fibres, Geobacillus thermoglucosidasius strain PB94A. Appl Microbiol Biotechnol 83:521–527. CrossRefGoogle Scholar
  55. Kämpfer P, Glaeser SP, Busse H–J (2013) Transfer of Bacillus schlegelii to a novel genus and proposal of Hydrogenibacillus schlegelii gen. nov., comb. nov. Int J Syst Evol Microbiol 63:1723–1727. CrossRefPubMedGoogle Scholar
  56. Kananavičiūtė R, Čitavičius D (2015) Genetic engineering of Geobacillus spp. J Microbiol Methods 111:31–39. CrossRefPubMedGoogle Scholar
  57. Kim P, Lee J, Park D, Shin K, Kim J, Kim C (2012) Gracilibacillus bigeumensis sp. nov., a moderately halophilic bacterium from solar saltern soil. Int J Syst Evol Microbiol 62:1857–1863. CrossRefPubMedGoogle Scholar
  58. Kim S, Lee J, Han S, Whang K (2015) Halobacillus sediminis sp. nov., a moderately halophilic bacterium isolated from a solar saltern sediment. Int J Syst Evol Microbiol 65:4434–4440. CrossRefPubMedGoogle Scholar
  59. Kinfu BM, Jahnke M, Janus M, Besirlioglu V, Roggenbuck M, Meurer R, Vojcic L, Borchert M, Schwaneberg U, Chow J, Streit WR (2017) Recombinant RNA polymerase from Geobacillus sp. GHH01 as tool for rapid generation of metagenomic RNAs using in vitro technologies. Biotechnol Bioeng 114:2739–2752. CrossRefPubMedGoogle Scholar
  60. Kobayashi J, Furukawa M, Ohshiro T, Suzuki H (2015a) Thermoadaptation-directed evolution of chloramphenicol acetyltransferase in an error-prone thermophile using improved procedures. Appl Microbiol Biotechnol 99:5563–5572. CrossRefPubMedGoogle Scholar
  61. Kobayashi J, Tanabiki M, Doi S, Kondo A, Ohshiro T, Suzuki H (2015b) Unique plasmids generated via pUC replicon mutagenesis in an error-prone thermophile derived from Geobacillus kaustophilus HTA426. Appl Environ Microbiol 81:7625–7632. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Kuisiene N, Raugalas J, Chitavichius D (2004) Geobacillus lituanicus sp. nov. Int J Syst Evol Microbiol 54:1991–1995. CrossRefPubMedGoogle Scholar
  63. La Duc MT, Dekas A, Osman S, Moissl C, Newcombe D, Venkateswaran K (2007) Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Appl Environ Microbiol 73:2600–2611. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Lambros RJ, Mortimer JR, Forsdyke DR (2003) Optimum growth temperature and the base composition of open reading frames in prokaryotes. Extremophiles 7:443–450. CrossRefPubMedGoogle Scholar
  65. Liao H, McKenzie T, Hageman R (1986) Isolation of a thermostable enzyme variant by cloning and selection in a thermophile. Proc Natl Acad Sci U S A 83:576–580. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Marchant R, Banat IM, Rahman TJ, Berzano M (2002) The frequency and characteristics of highly thermophilic bacteria in cool soil environments. Environ Microbiol 4:595–602. CrossRefPubMedGoogle Scholar
  67. Marchant R, Franzetti A, Pavlostathis SG, Tas DO, Erdbrügger I, Ünyayar A, Mazmanci MA, Banat IM (2008) Thermophilic bacteria in cool temperate soils: are they metabolically active or continually added by global atmospheric transport? Appl Microbiol Biotechnol 78:841–852. CrossRefPubMedGoogle Scholar
  68. 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 260:5298–5303Google Scholar
  69. McMullan G, Christie JM, Rahman TJ, Banat IM, Ternan NG, Marchant R (2004) Habitat, applications and genomics of the aerobic, thermophilic genus Geobacillus. Biochem Soc Trans 32:214–217. CrossRefPubMedGoogle Scholar
  70. Miñana-Galbis D, Pinzón DL, Lorén JG, Manresa A, Oliart-Ros RM (2010) Reclassification of Geobacillus pallidus (Scholz et al. 1988) Banat et al. 2004 as Aeribacillus pallidus gen. nov., comb. nov. Int J Syst Evol Microbiol 60:1600–1604. CrossRefPubMedGoogle Scholar
  71. Mizuno T, Ohshiro T, Suzuki H (2017) Plasmid curing is a promising approach to improve thermophiles for biotechnological applications: perspectives in archaea. In: Sghaier H (ed) Archaea - new biocatalysts, novel pharmaceuticals and various biotechnological applications. InTech, Rijeka, pp 83–99. Google Scholar
  72. Mougiakos I, Mohanraju P, Bosma EF, Vrouwe V, Bou MF, Naduthodi MIS, Gussak A, Brinkman RBL, van Kranenburg R, van der Oost J (2017) Characterizing a thermostable Cas9 for bacterial genome editing and silencing. Nat Commun 8:1647.
  73. Muhd Sakaff MKL, Abdul Rahman AY, Saito JA, Hou SB, Alam M (2011) Complete genome sequence of the thermophilic bacterium Geobacillus thermoleovorans CCB_US3_UF5. J Bacteriol 194:1239–1239. CrossRefGoogle Scholar
  74. Nazina TN, Tourova TP, Poltaraus AB, Novikova EV, Grigoryan AA, Ivanova AE, Lysenko AM, Petrunyaka VV, Osipov GA, Belyaev SS, Ivanov MV (2001) Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius, and G. thermodenitrificans. Int J Syst Evol Microbiol 51:433–446. CrossRefPubMedGoogle Scholar
  75. Nazina TN, Sokolova DS, Grigoryan AA, Shestakova NM, Mikhailova EM, Poltaraus AB, Tourova TP, Lysenko AM, Osipov GA, Belyaev SS (2005) Geobacillus jurassicus sp. nov., a new thermophilic bacterium isolated from a high-temperature petroleum reservoir, and the validation of the Geobacillus species. Syst Appl Microbiol 28:43–53. CrossRefPubMedGoogle Scholar
  76. Ortiz EM, Berretta MF, Navas LE, Benintende GB, Amadio AF, Zandomeni RO (2015) Draft genome sequence of Geobacillus sp. isolate T6, a thermophilic bacterium collected from a thermal spring in Argentina. Genome Announc 3:e00743–15. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Perfumo A, Marchant R (2010) Global transport of thermophilic bacteria in atmospheric dust. Environ Microbiol Rep 2:333–339. CrossRefPubMedGoogle Scholar
  78. Petkauskaite R, Blom J, Goesmann A, Kuisiene N (2017) Draft genome sequence of pectic polysaccharide-degrading moderate thermophilic bacterium Geobacillus thermodenitrificans DSM 101594. Braz J Microbiol 48:7–8. CrossRefPubMedGoogle Scholar
  79. Poli A, Romano I, Caliendo G, Nicolaus G, Orlando P, de Falco A, Lama L, Gambacorta A, Nicolaus B (2006) Geobacillus toebii subsp. decanicus subsp. nov., a hydrocarbon-degrading, heavy metal resistant bacterium from hot compost. J Gen Appl Microbiol 52:223–234. CrossRefPubMedGoogle Scholar
  80. Poli A, Guven K, Romano I, Pirinccioglu H, Guven RG, Euzeby JPM, Matpan F, Acer O, Orlando P, Nicolaus B (2012) Geobacillus subterraneus subsp. aromaticivorans subsp. nov., a novel thermophilic and alkaliphilic bacterium isolated from a hot spring in Sirnak, Turkey. J Gen Appl Microbiol 58:437–446. CrossRefPubMedGoogle Scholar
  81. Rahman TJ, Marchant R, Banat IM (2004) Distribution and molecular investigation of highly thermophilic bacteria associated with cool soil environments. Biochem Soc Trans 32:209–213. CrossRefPubMedGoogle Scholar
  82. Ren B, Yang N, Wang J, Ma X, Wang Q, Xie F, Guo H, Liu Z, Pugin B, Zhang L (2013) Amphibacillus marinus sp. nov., a member of the genus Amphibacillus isolated from marine mud. Int J Syst Evol Microbiol 63:1485–1491. CrossRefPubMedGoogle Scholar
  83. Romano I, Poli A, Lama L, Gambacorta A, Nicolaus B (2005) Geobacillus thermoleovorans subsp. stromboliensis subsp. nov., isolated from the geothermal volcanic environment. J Gen Appl Microbol 51:183–189. CrossRefGoogle Scholar
  84. Rozanov A, Logacheva MD, Peltek SE (2014) Draft genome sequences of Geobacillus stearothermophilus strains 22 and 53, isolated from the Garga hot spring in the Barguzin river valley of the Russian Federation. Genome Announc 2:e01205–14. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Sabath N, Ferrada E, Barve A, Wagner A (2013) Growth temperature and genome size in bacteria are negatively correlated, suggesting genomic streamlining during thermal adaptation. Genome Biol Evol 5:966–977. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Savery NJ (2007) The molecular mechanism of transcription-coupled DNA repair. Trends Microbiol 15:326–333. CrossRefPubMedGoogle Scholar
  87. Schlesner H, Lawson PA, Collins MD, Weiss N, Wehmeyer U, Völker H, Thomm M (2001) Filobacillus milensis gen. nov., sp. nov., a new halophilic spore-forming bacterium with Orn-D-Glu-type peptidoglycan. Int J Syst Evol Microbiol 51:425–431. CrossRefPubMedGoogle Scholar
  88. Shahinyan G, Margaryan A, Panosyan H, Trchounian A (2017) Identification and sequence analyses of novel lipase encoding novel thermophillic bacilli isolated from Armenian geothermal springs. BMC Microbiol 17:103.
  89. Shimura M, Mukerjee-Dhar G, Kimbara K, Nagato H, Kiyohara H, Hatta T (1999) Isolation and characterization of a thermophilic Bacillus sp. JF8 capable of degrading polychlorinated biphenyls and naphthalene. FEMS Microbiol Lett 178:87–93. CrossRefPubMedGoogle Scholar
  90. Siddiqui MA, Rashid N, Ayyampalayam S, Whitman WB (2014) Draft genome sequence of Geobacillus thermopakistaniensis strain MAS1. Genome Announc 2:e00559–14.
  91. Sieber V, Plückthun A, Schmid FX (1998) Selecting proteins with improved stability by a phage-based method. Nat Biotechnol 16:955–960. CrossRefPubMedGoogle Scholar
  92. Sood N, Lal B (2008) Isolation and characterization of a potential paraffin-wax degrading thermophilic bacterial strain Geobacillus kaustophilus TERI NSM for application in oil wells with paraffin deposition problems. Chemosphere 70:1445–1451. CrossRefPubMedGoogle Scholar
  93. de Souza YPA, da Mota FF, Rosado AS (2017) Draft genome sequence of Geobacillus sp. LEMMY01, a thermophilic bacterium isolated from the site of a burning grass pile. Genome Announc 5:e00200–17.
  94. Stackebrandt E, Ludwig W, Weizenegger M, Dorn S, McGill TJ, Fox GE, Woese CR, Schubert W, Schleifer K (1987) Comparative 16S rRNA oligonucleotide analyses and murein types of round-spore-forming bacilli and non-spore-forming relatives. J Gen Microbiol 133:2523–2529. CrossRefPubMedGoogle Scholar
  95. Studholme DJ (2015) Some (bacilli) like it hot: genomics of Geobacillus species. Microbial Biotechnol 8:40–48. CrossRefGoogle Scholar
  96. Studholme DJ, Jackson RA, Leak DJ (1999) Phylogenetic analysis of transformable strains of thermophilic Bacillus species. FEMS Microbiol Lett 172:85–90. CrossRefPubMedGoogle Scholar
  97. Stuknyte M, Guglielmetti S, Mora D, Kuisiene N, Parini C, Citavicius D (2008) Complete nucleotide sequence of pGS18, a 62.8-kb plasmid from Geobacillus stearothermophilus strain 18. Extremophiles 12:415–429. CrossRefPubMedGoogle Scholar
  98. Sultanpuram VR, Mothe T (2016) Salipaludibacillus aurantiacus gen. nov., sp. nov. a novel alkali tolerant bacterium, reclassification of Bacillus agaradhaerens as Salipaludibacillus agaradhaerens comb. nov. and Bacillus neizhouensis as Salipaludibacillus neizhouensis comb. nov. Int J Syst Evol Microbiol 66:2747–2753. CrossRefPubMedGoogle Scholar
  99. Sun Y, Ning Z, Yang F, Li X (2015) Characteristics of newly isolated Geobacillus sp. ZY-10 degrading hydrocarbons in crude oil. Pol J Microbiol 64:253–263CrossRefGoogle Scholar
  100. Suzuki H (2017) Geobacillus kaustophilus HTA426: a model organism for moderate thermophiles. In: Berhardt LV (ed) Advances in medicine and biology. Nova Science Publishers, New York, pp 75–108Google Scholar
  101. Suzuki H, Kobayashi J, Wada K, Furukawa M, Doi K (2015) Thermoadaptation-directed enzyme evolution in an error-prone thermophile derived from Geobacillus kaustophilus HTA426. Appl Environ Microbiol 81:149–158. CrossRefPubMedGoogle Scholar
  102. Suzuki H, Taketani T, Kobayashi J, Ohshiro T (2018) Antibiotic resistance mutations induced in growing cells of Bacillus-related thermophiles. J Antibiot 71:382–389. CrossRefPubMedGoogle Scholar
  103. Takami H, Inoue A, Fuji F, Horikoshi K (1997) Microbial flora in the deepest sea mud of the Mariana Trench. FEMS Microbiol Lett 152:279–285. CrossRefPubMedGoogle Scholar
  104. Takami H, Takaki Y, Chee GJ, Nishi S, Shimamura S, Suzuki H, Matsui S, Uchiyama I (2004) Thermoadaptation trait revealed by the genome sequence of thermophilic Geobacillus kaustophilus. Nucleic Acids Res 32:6292–6303. CrossRefPubMedPubMedCentralGoogle Scholar
  105. Tayyab M, Rashid N, Akhtar M (2011) Isolation and identification of lipase producing thermophilic Geobacillus sp. SBS-4S: cloning and characterization of the lipase. J Biosci Bioeng 111:272–278. CrossRefPubMedGoogle Scholar
  106. Wada K, Kobayashi J, Furukawa M, Doi K, Ohshiro T, Suzuki H (2016) A thiostrepton resistance gene and its mutants serve as selectable markers in Geobacillus kaustophilus HTA426. Biosci Biotechnol Biochem 80:368–375. CrossRefPubMedGoogle Scholar
  107. Wang L, Tang Y, Wang S, Liu R, Liu M, Zhang Y, Liang F, Feng L (2006) Isolation and characterization of a novel thermophilic Bacillus strain degrading long-chain n-alkanes. Extremophiles 10:347–356. CrossRefPubMedGoogle Scholar
  108. White D, Sharp RJ, Priest FG (1993) A polyphasic taxonomic geographical area study of thermophilic bacilli from a wide geographical area. Antonie Van Leeuwenhoek 64:357–386CrossRefGoogle Scholar
  109. Wiegand S, Rabausch U, Chow J, Daniel R, Streit WR, Lieseganga H (2013) Complete genome sequence of Geobacillus sp. strain GHH01, a thermophilic lipase-secreting bacterium. Genome Announc 1:e0009213.
  110. Wiegel J, Ljungdahl LG (1986) The importance of thermophilic bacteria in biotechnology. Crit Rev Biotechnol 3:39–108CrossRefGoogle Scholar
  111. Wissuwa J, Stokke R, Fedøy A, Lian K, Smalås AO, Steen IH (2016) Isolation and complete genome sequence of the thermophilic Geobacillus sp. 12AMOR1 from an Arctic deep-sea hydrothermal vent site. Stand Genomic Sci 11:16.
  112. Xu K, He Z, Mao Y, Sheng R, Sheng Z (1993) On two transposable elements from Bacillus stearothermophilus. Plasmid 29:1–9. CrossRefPubMedGoogle Scholar
  113. Yang SH, Cho J, Lee S, Abanto OD, Kim S, Ghosh C, Lim J, Hwang S (2013) Isolation and characterization of novel denitrifying bacterium Geobacillus sp. SG-01 strain from wood chips composted with swine manure. Asian-Australas J Anim Sci 26:1651–1658. CrossRefPubMedPubMedCentralGoogle Scholar
  114. Yoshida K, Sanbongi A, Murakami A, Suzuki H, Takenaka S, Takami H (2012) Three inositol dehydrogenases involved in utilization and interconversion of inositol stereoisomers in a thermophile, Geobacillus kaustophilus HTA426. Microbiology 158:1942–1952. CrossRefPubMedGoogle Scholar
  115. Zeigler DR (2001) The genus Geobacillus: Bacillus genetic stock center catalog of strains, 7th edn, vol 3. Bacillus genetic stock center, ColumbusGoogle Scholar
  116. Zeigler DR (2005) Application of a recN sequence similarity analysis to the identification of species within the bacterial genus Geobacillus. Int J Syst Evol Microbiol 55:1171–1179. CrossRefPubMedGoogle Scholar
  117. Zeigler DR (2014) The Geobacillus paradox: why is a thermophilic bacterial genus so prevalent on a mesophilic planet? Microbiology 160:1–11. CrossRefPubMedGoogle Scholar
  118. Zhang J, Zhang X, Liu J, Li R, Shen B (2012) Isolation of a thermophilic bacterium, Geobacillus sp. SH-1, capable of degrading aliphatic hydrocarbons and naphthalene simultaneously, and identification of its naphthalene degrading pathway. Bioresour Technol 124:83–89. CrossRefPubMedGoogle Scholar
  119. Zhu L, Li M, Guo S, Wang W (2016) Draft genome sequence of a thermophilic desulfurization bacterium, Geobacillus thermoglucosidasius strain W-2. Genome Announc 4:e00793–16.
  120. Zhu Y, Wang G, Ni H, Xiao A, Cai H (2014) Cloning and characterization of a new manganese superoxide dismutase from deep-sea thermophile Geobacillus sp. EPT3. World J Microbiol Biotechnol 30:1347–1357. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of EngineeringTottori UniversityTottoriJapan
  2. 2.Centre for Research on Green Sustainable ChemistryTottori UniversityTottoriJapan

Personalised recommendations