1887

Abstract

The genus comprises endospore-forming obligate thermophiles. These bacteria have been isolated from cool soils and even cold ocean sediments in anomalously high numbers, given that the ambient temperatures are significantly below their minimum requirement for growth. Geobacilli are active in environments such as hot plant composts, however, and examination of their genome sequences reveals that they are endowed with a battery of sensors, transporters and enzymes dedicated to hydrolysing plant polysaccharides. Although they appear to be relatively minor members of the plant biomass-degrading microbial community, bacteria have achieved a significant population with a worldwide distribution, probably in large part due to adaptive features of their spores. First, their morphology and resistance properties enable them to be mobilized in the atmosphere and transported long distances. Second, their longevity, which in theory may be extreme, enables them to lie quiescent but viable for long periods of time, accumulating gradually over time to achieve surprisingly high population densities.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.071696-0
2014-01-01
2020-01-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/1/1.html?itemId=/content/journal/micro/10.1099/mic.0.071696-0&mimeType=html&fmt=ahah

References

  1. Abdel-Fattah Y. R., Gaballa A. A.. ( 2008;). Identification and over-expression of a thermostable lipase from Geobacillus thermoleovorans Toshki in Escherichia coli . Microbiol Res163:13–20 [CrossRef][PubMed]
    [Google Scholar]
  2. Abu-Zinada A. H., Hossain A., Yonis H. I., Elwan S. H.. ( 1981;). Bacillus stearothermophilus from Saudi Arabian soils. Folia Microbiol (Praha)26:364–369 [CrossRef][PubMed]
    [Google Scholar]
  3. Al-Hassan J. M., Al-Awadi S., Oommen S., Alkhamis A., Afzal M.. ( 2011;). Tryptophan oxidative metabolism catalyzed by Geobacillus stearothermophilus: a thermophile isolated from Kuwait soil contaminated with petroleum hydrocarbons. Int J Tryptophan Res4:1–6[PubMed]
    [Google Scholar]
  4. Ariatti A., Comtois P.. ( 1993;). Louis Pasteur: the first experimental aerobiologist. Aerobiologia9:5–14 [CrossRef]
    [Google Scholar]
  5. Bartholomew J. W., Paik G.. ( 1966;). Isolation and identification of obligate thermophilic sporeforming bacilli from ocean basin cores. J Bacteriol92:635–638[PubMed]
    [Google Scholar]
  6. Belda E., Sekowska A., Le Fèvre F., Morgat A., Mornico D., Ouzounis C., Vallenet D., Médigue C., Danchin A.. ( 2013;). An updated metabolic view of the Bacillus subtilis 168 genome. Microbiology159:757–770 [CrossRef][PubMed]
    [Google Scholar]
  7. Blanc M., Marilley L., Beffa T., Aragno M.. ( 1997;). Rapid identification of heterotrophic, thermophilic, spore-forming bacteria isolated from hot composts. Int J Syst Bacteriol47:1246–1248 [CrossRef][PubMed]
    [Google Scholar]
  8. Blom J., Albaum S. P., Doppmeier D., Pühler A., Vorhölter F. J., Zakrzewski M., Goesmann A.. ( 2009;). edgar: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics10:154 [CrossRef][PubMed]
    [Google Scholar]
  9. Bowers R. M., Sullivan A. P., Costello E. K., Collett J. L. Jr, Knight R., Fierer N.. ( 2011;). Sources of bacteria in outdoor air across cities in the midwestern United States. Appl Environ Microbiol77:6350–6356 [CrossRef][PubMed]
    [Google Scholar]
  10. Brodie E. L., DeSantis T. Z., Parker J. P., Zubietta I. X., Piceno Y. M., Andersen G. L.. ( 2007;). Urban aerosols harbor diverse and dynamic bacterial populations. Proc Natl Acad Sci U S A104:299–304 [CrossRef][PubMed]
    [Google Scholar]
  11. Burrows S. M., Butler T., Jöckel P., Tost H., Kerkweg A., Pöschl U., Lawrence M. G.. ( 2009a;). Bacteria in the global atmosphere – part 2: modeling of emissions and transport between different ecosystems. Atmos Chem Phys9:9281–9297 [CrossRef]
    [Google Scholar]
  12. Burrows S. M., Elbert W., Lawrence M. G., Pöschl U.. ( 2009b;). Bacteria in the global atmosphere: part 1 – review and synthesis of literature data for different ecosystems. Atmos Chem Phys9:9263–9280 [CrossRef]
    [Google Scholar]
  13. Canakci S., Inan K., Kacagan M., Belduz A. O.. ( 2007;). Evaluation of arabinofuranosidase and xylanase activities of Geobacillus spp. isolated from some hot springs in Turkey. J Microbiol Biotechnol17:1262–1270[PubMed]
    [Google Scholar]
  14. Cebrian J.. ( 1999;). Patterns in the fate of production in plant communities. Am Nat154:449–468 [CrossRef][PubMed]
    [Google Scholar]
  15. Commichau F. M., Pietack N., Stülke J.. ( 2013;). Essential genes in Bacillus subtilis: a re-evaluation after ten years. Mol Biosyst9:1068–1075 [CrossRef][PubMed]
    [Google Scholar]
  16. Cripps R. E., Eley K., Leak D. J., Rudd B., Taylor M., Todd M., Boakes S., Martin S., Atkinson T.. ( 2009;). Metabolic engineering of Geobacillus thermoglucosidasius for high yield ethanol production. Metab Eng11:398–408 [CrossRef][PubMed]
    [Google Scholar]
  17. de Champdoré M., Staiano M., Rossi M., D’Auria S.. ( 2007;). Proteins from extremophiles as stable tools for advanced biotechnological applications of high social interest. J R Soc Interface4:183–191 [CrossRef][PubMed]
    [Google Scholar]
  18. DeFlaun M. F., Fredrickson J. K., Dong H., Pfiffner S. M., Onstott T. C., Balkwill D. L., Streger S. H., Stackebrandt E., Knoessen S., van Heerden E.. ( 2007;). Isolation and characterization of a Geobacillus thermoleovorans strain from an ultra-deep South African gold mine. Syst Appl Microbiol30:152–164 [CrossRef][PubMed]
    [Google Scholar]
  19. DeLeon-Rodriguez N., Lathem T. L., Rodriguez-R L. M., Barazesh J. M., Anderson B. E., Beyersdorf A. J., Ziemba L. D., Bergin M., Nenes A., Konstantinidis K. T.. ( 2013;). Microbiome of the upper troposphere: species composition and prevalence, effects of tropical storms, and atmospheric implications. Proc Natl Acad Sci U S A110:2575–2580 [CrossRef][PubMed]
    [Google Scholar]
  20. Derekova A., Sjøholm C., Mandeva R., Michailova L., Kambourova M.. ( 2006;). Biosynthesis of a thermostable gellan lyase by newly isolated and characterized strain of Geobacillus stearothermophilus 98. Extremophiles10:321–326 [CrossRef][PubMed]
    [Google Scholar]
  21. Donk P. J.. ( 1920;). A highly resistant thermophilic organism. J Bacteriol5:373–374[PubMed]
    [Google Scholar]
  22. Driks A.. ( 2002;). Maximum shields: the assembly and function of the bacterial spore coat. Trends Microbiol10:251–254 [CrossRef][PubMed]
    [Google Scholar]
  23. Fields M. L., Chen Lee P. P.. ( 1974;). Bacillus stearothermophilus in soils of Iceland. Appl Microbiol28:638–640[PubMed]
    [Google Scholar]
  24. Fortina M. G., Mora D., Schumann P., Parini C., Manachini P. L., Stackebrandt E.. ( 2001;). Reclassification of Saccharococcus caldoxylosilyticus as Geobacillus caldoxylosilyticus (Ahmad et al. 2000) comb. nov.. Int J Syst Evol Microbiol51:2063–2071 [CrossRef][PubMed]
    [Google Scholar]
  25. Fujita M., Losick R.. ( 2005;). Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev19:2236–2244 [CrossRef][PubMed]
    [Google Scholar]
  26. Fujita M., González-Pastor J. E., Losick R.. ( 2005;). High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis . J Bacteriol187:1357–1368 [CrossRef][PubMed]
    [Google Scholar]
  27. Galperin M. Y., Mekhedov S. L., Puigbo P., Smirnov S., Wolf Y. I., Rigden D. J.. ( 2012;). Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ Microbiol14:2870–2890 [CrossRef][PubMed]
    [Google Scholar]
  28. Gilbert H. J.. ( 2010;). The biochemistry and structural biology of plant cell wall deconstruction. Plant Physiol153:444–455 [CrossRef][PubMed]
    [Google Scholar]
  29. Griffin D. W.. ( 2007;). Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin Microbiol Rev20:459–477 [CrossRef][PubMed]
    [Google Scholar]
  30. Griffin D. W., Garrison V. H., Herman J. R., Shinn E. A.. ( 2001;). African desert dust in the Caribbean atmosphere: microbiology and public health. Aerobiologia17:203–213 [CrossRef]
    [Google Scholar]
  31. Griffin D. W., Kellogg C. A., Garrison V. H., Lisle J. T., Borden T. C., Shinn E. A.. ( 2003;). Atmospheric microbiology in the northern Caribbean during African dust events. Aerobiologia19:143–157 [CrossRef]
    [Google Scholar]
  32. Griffin D. W., Westphal D. L., Gray M. A.. ( 2006;). Airborne microorganisms in the African desert dust corridor over the mid-Atlantic ridge, Ocean Drilling Program, leg 209. Aerobiologia22:211–226 [CrossRef]
    [Google Scholar]
  33. Hondoh H., Kuriki T., Matsuura Y.. ( 2003;). Three-dimensional structure and substrate binding of Bacillus stearothermophilus neopullulanase. J Mol Biol326:177–188 [CrossRef][PubMed]
    [Google Scholar]
  34. Hua N. P., Kobayashi F., Iwasaka Y., Shi G. Y., Naganuma T.. ( 2007;). Detailed identification of desert-originated bacteria carried by Asian dust storms to Japan. Aerobiologia23:291–298 [CrossRef]
    [Google Scholar]
  35. Johnson S. S., Hebsgaard M. B., Christensen T. R., Mastepanov M., Nielsen R., Munch K., Brand T., Gilbert M. T., Zuber M. T.. & other authors ( 2007;). Ancient bacteria show evidence of DNA repair. Proc Natl Acad Sci U S A104:14401–14405 [CrossRef][PubMed]
    [Google Scholar]
  36. Karagüler N. G., Sessions R. B., Binay B., Ordu E. B., Clarke A. R.. ( 2007;). Protein engineering applications of industrially exploitable enzymes: Geobacillus stearothermophilus LDH and Candida methylica FDH. Biochem Soc Trans35:1610–1615 [CrossRef][PubMed]
    [Google Scholar]
  37. Kato T., Haruki M., Imanaka T., Morikawa M., Kanaya S.. ( 2001;). Isolation and characterization of long-chain-alkane degrading Bacillus thermoleovorans from deep subterranean petroleum reservoirs. J Biosci Bioeng91:64–70[PubMed][CrossRef]
    [Google Scholar]
  38. Kellogg C. A., Griffin D. W.. ( 2006;). Aerobiology and the global transport of desert dust. Trends Ecol Evol21:638–644 [CrossRef][PubMed]
    [Google Scholar]
  39. Kennedy M. J., Reader S. L., Swierczynski L. M.. ( 1994;). Preservation records of micro-organisms: evidence of the tenacity of life. Microbiology140:2513–2529 [CrossRef][PubMed]
    [Google Scholar]
  40. Khasin A., Alchanati I., Shoham Y.. ( 1993;). Purification and characterization of a thermostable xylanase from Bacillus stearothermophilus T-6. Appl Environ Microbiol59:1725–1730[PubMed]
    [Google Scholar]
  41. Kimura H., Asada R., Masta A., Naganuma T.. ( 2003;). Distribution of microorganisms in the subsurface of the Manus Basin hydrothermal vent field in Papua New Guinea. Appl Environ Microbiol69:644–648 [CrossRef][PubMed]
    [Google Scholar]
  42. Klämpfl T. G., Isbary G., Shimizu T., Li Y. F., Zimmermann J. L., Stolz W., Schlegel J., Morfill G. E., Schmidt H. U.. ( 2012;). Cold atmospheric air plasma sterilization against spores and other microorganisms of clinical interest. Appl Environ Microbiol78:5077–5082 [CrossRef][PubMed]
    [Google Scholar]
  43. Lai X., Ingram L. O.. ( 1993;). Cloning and sequencing of a cellobiose phosphotransferase system operon from Bacillus stearothermophilus XL-65-6 and functional expression in Escherichia coli . J Bacteriol175:6441–6450[PubMed]
    [Google Scholar]
  44. Lama L., Calandrelli V., Gambacorta A., Nicolaus B.. ( 2004;). Purification and characterization of thermostable xylanase and β-xylosidase by the thermophilic bacterium Bacillus thermantarcticus . Res Microbiol155:283–289 [CrossRef][PubMed]
    [Google Scholar]
  45. Lambert R. J.. ( 2003;). A model for the thermal inactivation of micro-organisms. J Appl Microbiol95:500–507 [CrossRef][PubMed]
    [Google Scholar]
  46. Le Goff O., Bru-Adan V., Bacheley H., Godon J. J., Wéry N.. ( 2010;). The microbial signature of aerosols produced during the thermophilic phase of composting. J Appl Microbiol108:325–340 [CrossRef][PubMed]
    [Google Scholar]
  47. Lindahl T.. ( 1993;). Instability and decay of the primary structure of DNA. Nature362:709–715 [CrossRef][PubMed]
    [Google Scholar]
  48. Liu B., Wu S., Song Q., Zhang X., Xie L.. ( 2006;). Two novel bacteriophages of thermophilic bacteria isolated from deep-sea hydrothermal fields. Curr Microbiol53:163–166 [CrossRef][PubMed]
    [Google Scholar]
  49. Mäder U., Schmeisky A. G., Flórez L. A., Stülke J.. ( 2012;). SubtiWiki – a comprehensive community resource for the model organism Bacillus subtilis . Nucleic Acids Res40:Database issueD1278–D1287 [CrossRef][PubMed]
    [Google Scholar]
  50. Marchant R., Banat I. M., Rahman T. J., Berzano M.. ( 2002;). The frequency and characteristics of highly thermophilic bacteria in cool soil environments. Environ Microbiol4:595–602 [CrossRef][PubMed]
    [Google Scholar]
  51. Marchant R., Franzetti A., Pavlostathis S. G., Tas D. O., Erdbrugger I., Unyayar A., Mazmanci M. A., Banat I. M.. ( 2008;). Thermophilic bacteria in cool temperate soils: are they metabolically active or continually added by global atmospheric transport. Appl Microbiol Biotechnol78:841–852 [CrossRef][PubMed]
    [Google Scholar]
  52. Markossian S., Becker P., Märkl H., Antranikian G.. ( 2000;). Isolation and characterization of lipid-degrading Bacillus thermoleovorans IHI-91 from an Icelandic hot spring. Extremophiles4:365–371 [CrossRef][PubMed]
    [Google Scholar]
  53. Marquis R. E., Bender G. R.. ( 1985;). Mineralization and heat resistance of bacterial spores. J Bacteriol161:789–791[PubMed]
    [Google Scholar]
  54. Martins L. F., Antunes L. P., Pascon R. C., de Oliveira J. C., Digiampietri L. A., Barbosa D., Peixoto B. M., Vallim M. A., Viana-Niero C.. & other authors ( 2013;). Metagenomic analysis of a tropical composting operation at the São Paulo Zoo Park reveals diversity of biomass degradation functions and organisms. PLoS ONE8:e61928 [CrossRef][PubMed]
    [Google Scholar]
  55. Maugeri T. L., Gugliandolo C., Caccamo D., Stackebrandt E.. ( 2001;). A polyphasic taxonomic study of thermophilic bacilli from shallow, marine vents. Syst Appl Microbiol24:572–587 [CrossRef][PubMed]
    [Google Scholar]
  56. Meintanis C., Chalkou K. I., Kormas K. A., Karagouni A. D.. ( 2006;). Biodegradation of crude oil by thermophilic bacteria isolated from a volcano island. Biodegradation17:105–111 [CrossRef][PubMed]
    [Google Scholar]
  57. Michel F. C. Jr, Marsh T. J., Reddy C. A.. ( 2002;). Bacterial community structure during yard trimmings composting. Microbiology of Composting25–42 Insam H., Riddech M., Klammer S.. Berlin: Springer; [CrossRef]
    [Google Scholar]
  58. Moeller R., Setlow P., Horneck G., Berger T., Reitz G., Rettberg P., Doherty A. J., Okayasu R., Nicholson W. L.. ( 2008;). Roles of the major, small, acid-soluble spore proteins and spore-specific and universal DNA repair mechanisms in resistance of Bacillus subtilis spores to ionizing radiation from X rays and high-energy charged-particle bombardment. J Bacteriol190:1134–1140 [CrossRef][PubMed]
    [Google Scholar]
  59. Mosley G. A., Gillis J. R., Krushefski G.. ( 2005;). Evaluating the formulae for integrated lethality in ethylene oxide sterilization using six different endospore forming strains of bacteria, and comparisons of integrated lethality for ethylene oxide and steam systems. PDA J Pharm Sci Technol59:64–86[PubMed]
    [Google Scholar]
  60. Muhd Sakaff M. K., Abdul Rahman A. Y., Saito J. A., Hou S., Alam M.. ( 2012;). Complete genome sequence of the thermophilic bacterium Geobacillus thermoleovorans CCB_US3_UF5. J Bacteriol194:1239 [CrossRef][PubMed]
    [Google Scholar]
  61. Nazina T. N., Tourova T. P., Poltaraus A. B., Novikova E. V., Grigoryan A. A., Ivanova A. E., Lysenko A. M., Petrunyaka V. V., Osipov G. A.. & other authors ( 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 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 Microbiol51:433–446[PubMed]
    [Google Scholar]
  62. Nicholson W. L.. ( 2003;). Using thermal inactivation kinetics to calculate the probability of extreme spore longevity: implications for paleomicrobiology and lithopanspermia. Orig Life Evol Biosph33:621–631 [CrossRef][PubMed]
    [Google Scholar]
  63. Nicholson W. L., Munakata N., Horneck G., Melosh H. J., Setlow P.. ( 2000;). Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev64:548–572 [CrossRef][PubMed]
    [Google Scholar]
  64. O’Malley M. A.. ( 2008;). ‘Everything is everywhere: but the environment selects’: ubiquitous distribution and ecological determinism in microbial biogeography. Stud Hist Philos Biol Biomed Sci39:314–325 [CrossRef][PubMed]
    [Google Scholar]
  65. Obojska A., Ternan N. G., Lejczak B., Kafarski P., McMullan G.. ( 2002;). Organophosphonate utilization by the thermophile Geobacillus caldoxylosilyticus T20. Appl Environ Microbiol68:2081–2084 [CrossRef][PubMed]
    [Google Scholar]
  66. Partanen P., Hultman J., Paulin L., Auvinen P., Romantschuk M.. ( 2010;). Bacterial diversity at different stages of the composting process. BMC Microbiol10:94 [CrossRef][PubMed]
    [Google Scholar]
  67. Pavlostathis S. G., Marchant R., Banat I. M., Ternan N. G., McMullan G.. ( 2006;). High growth rate and substrate exhaustion results in rapid cell death and lysis in the thermophilic bacterium Geobacillus thermoleovorans . Biotechnol Bioeng95:84–95 [CrossRef][PubMed]
    [Google Scholar]
  68. Perfumo A., Marchant R.. ( 2010;). Global transport of thermophilic bacteria in atmospheric dust. Environ Microbiol Rep2:333–339 [CrossRef][PubMed]
    [Google Scholar]
  69. Perfumo A., Banat I. M., Marchant R., Vezzulli L.. ( 2007;). Thermally enhanced approaches for bioremediation of hydrocarbon-contaminated soils. Chemosphere66:179–184 [CrossRef][PubMed]
    [Google Scholar]
  70. Peters S., Koschinsky S., Schwieger F., Tebbe C. C.. ( 2000;). Succession of microbial communities during hot composting as detected by PCR-single-strand-conformation polymorphism-based genetic profiles of small-subunit rRNA genes. Appl Environ Microbiol66:930–936 [CrossRef][PubMed]
    [Google Scholar]
  71. Pinzón-Martínez D. L., Rodríguez-Gómez C., Miñana-Galbis D., Carrillo-Chávez J. A., Valerio-Alfaro G., Oliart-Ros R.. ( 2010;). Thermophilic bacteria from Mexican thermal environments: isolation and potential applications. Environ Technol31:957–966 [CrossRef][PubMed]
    [Google Scholar]
  72. Rahman T. J., Marchant R., Banat I. M.. ( 2004;). Distribution and molecular investigation of highly thermophilic bacteria associated with cool soil environments. Biochem Soc Trans32:209–213 [CrossRef][PubMed]
    [Google Scholar]
  73. Rastogi G., Muppidi G. L., Gurram R. N., Adhikari A., Bischoff K. M., Hughes S. R., Apel W. A., Bang S. S., Dixon D. J., Sani R. K.. ( 2009;). Isolation and characterization of cellulose-degrading bacteria from the deep subsurface of the Homestake gold mine, Lead, South Dakota, USA. J Ind Microbiol Biotechnol36:585–598 [CrossRef][PubMed]
    [Google Scholar]
  74. Reanprayoon P., Yoonaiwong W.. ( 2012;). Airborne concentrations of bacteria and fungi in Thailand border market. Aerobiologia28:49–60 [CrossRef]
    [Google Scholar]
  75. Rohde R., Muller R. A., Jacobsen R., Muller E., Perlmutter S., Rosenfeld A., Wurtele J., Groom D., Wickham C.. ( 2013;). A new estimate of the average earth surface land temperature spanning 1753 to 2011. Geoinfor Geostat: an Overview1:1
    [Google Scholar]
  76. Ronimus R. S., Parker L. E., Turner N., Poudel S., Rückert A., Morgan H. W.. ( 2003;). A RAPD-based comparison of thermophilic bacilli from milk powders. Int J Food Microbiol85:45–61 [CrossRef][PubMed]
    [Google Scholar]
  77. Rückert A., Ronimus R. S., Morgan H. W.. ( 2004;). A RAPD-based survey of thermophilic bacilli in milk powders from different countries. Int J Food Microbiol96:263–272 [CrossRef][PubMed]
    [Google Scholar]
  78. Ryckeboer J., Mergaert J., Vaes K., Klammer S., De Clercq D., Coosemans J., Insam H., Swings J.. ( 2003;). A survey of bacteria and fungi occurring during composting and self-heating processes. Ann Microbiol53:349–410
    [Google Scholar]
  79. Sadaie Y., Nakadate H., Fukui R., Yee L. M., Asai K.. ( 2008;). Glucomannan utilization operon of Bacillus subtilis . FEMS Microbiol Lett279:103–109 [CrossRef][PubMed]
    [Google Scholar]
  80. Saffary R., Nandakumar R., Spencer D., Robb F. T., Davila J. M., Swartz M., Ofman L., Thomas R. J., DiRuggiero J.. ( 2002;). Microbial survival of space vacuum and extreme ultraviolet irradiation: strain isolation and analysis during a rocket flight. FEMS Microbiol Lett215:163–168 [CrossRef][PubMed]
    [Google Scholar]
  81. Sankaranarayanan K., Timofeeff M. N., Spathis R., Lowenstein T. K., Lum J. K.. ( 2011;). Ancient microbes from halite fluid inclusions: optimized surface sterilization and DNA extraction. PLoS ONE6:e20683 [CrossRef][PubMed]
    [Google Scholar]
  82. Seale R. B., Dhakal R., Chauhan K., Craven H. M., Deeth H. C., Pillidge C. J., Powell I. B., Turner M. S.. ( 2012;). Genotyping of present-day and historical Geobacillus species isolates from milk powders by high-resolution melt analysis of multiple variable-number tandem-repeat loci. Appl Environ Microbiol78:7090–7097 [CrossRef][PubMed]
    [Google Scholar]
  83. Setlow P.. ( 2006;). Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol101:514–525 [CrossRef][PubMed]
    [Google Scholar]
  84. Sevenier V., Delannoy S., André S., Fach P., Remize F.. ( 2012;). Prevalence of Clostridium botulinum and thermophilic heat-resistant spores in raw carrots and green beans used in French canning industry. Int J Food Microbiol155:263–268 [CrossRef][PubMed]
    [Google Scholar]
  85. Shaffer B. T., Lighthart B.. ( 1997;). Survey of culturable airborne bacteria at four diverse locations in Oregon: urban, rural, forest, and coastal. Microb Ecol34:167–177 [CrossRef][PubMed]
    [Google Scholar]
  86. Shulami S., Gat O., Sonenshein A. L., Shoham Y.. ( 1999;). The glucuronic acid utilization gene cluster from Bacillus stearothermophilus T-6. J Bacteriol181:3695–3704[PubMed]
    [Google Scholar]
  87. Shulami S., Raz-Pasteur A., Tabachnikov O., Gilead-Gropper S., Shner I., Shoham Y.. ( 2011;). The l-arabinan utilization system of Geobacillus stearothermophilus . J Bacteriol193:2838–2850 [CrossRef][PubMed]
    [Google Scholar]
  88. Smith D. J., Griffin D. W.. ( 2013;). Inadequate methods and questionable conclusions in atmospheric life study. Proc Natl Acad Sci U S A110:E2084 [CrossRef][PubMed]
    [Google Scholar]
  89. Smith D. J., Jaffe D. A., Birmele M. N., Griffin D. W., Schuerger A. C., Hee J., Roberts M. S.. ( 2012;). Free tropospheric transport of microorganisms from Asia to North America. Microb Ecol64:973–985 [CrossRef][PubMed]
    [Google Scholar]
  90. Smith D. J., Timonen H. J., Jaffe D. A., Griffin D. W., Birmele M. N., Perry K. D., Ward P. D., Roberts M. S.. ( 2013;). Intercontinental dispersal of Bacteria and Archaea by transpacific winds. Appl Environ Microbiol79:1134–1139 [CrossRef][PubMed]
    [Google Scholar]
  91. Strom P. F.. ( 1985;). Effect of temperature on bacterial species diversity in thermophilic solid-waste composting. Appl Environ Microbiol50:899–905[PubMed]
    [Google Scholar]
  92. Struchtemeyer C. G., Davis J. P., Elshahed M. S.. ( 2011;). Influence of the drilling mud formulation process on the bacterial communities in thermogenic natural gas wells of the Barnett Shale. Appl Environ Microbiol77:4744–4753 [CrossRef][PubMed]
    [Google Scholar]
  93. Tabachnikov O., Shoham Y.. ( 2013;). Functional characterization of the galactan utilization system of Geobacillus stearothermophilus . FEBS J280:950–964[PubMed]
    [Google Scholar]
  94. Takaku H., Kodaira S., Kimoto A., Nashimoto M., Takagi M.. ( 2006;). Microbial communities in the garbage composting with rice hull as an amendment revealed by culture-dependent and -independent approaches. J Biosci Bioeng101:42–50 [CrossRef][PubMed]
    [Google Scholar]
  95. Takamatsu H., Watabe K.. ( 2002;). Assembly and genetics of spore protective structures. Cell Mol Life Sci59:434–444 [CrossRef][PubMed]
    [Google Scholar]
  96. Takami H., Nishi S., Lu J., Shimamura S., Takaki Y.. ( 2004;). Genomic characterization of thermophilic Geobacillus species isolated from the deepest sea mud of the Mariana Trench. Extremophiles8:351–356 [CrossRef][PubMed]
    [Google Scholar]
  97. Taylor M. P., Eley K. L., Martin S., Tuffin M. I., Burton S. G., Cowan D. A.. ( 2009;). Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Trends Biotechnol27:398–405 [CrossRef][PubMed]
    [Google Scholar]
  98. Tettelin H., Masignani V., Cieslewicz M. J., Donati C., Medini D., Ward N. L., Angiuoli S. V., Crabtree J., Jones A. L.. & other authors ( 2005;). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A102:13950–13955 [CrossRef][PubMed]
    [Google Scholar]
  99. Tong Y., Che F., Ku X., Chen M., Ye B., Li J.. ( 1993;). Population study of atmospheric bacteria at the Fengtai district of Beijing on two representative days. Aerobiologia9:69–74 [CrossRef]
    [Google Scholar]
  100. Wang L., Tang Y., Wang S., Liu R. L., Liu M. Z., Zhang Y., Liang F. L., Feng L.. ( 2006;). Isolation and characterization of a novel thermophilic Bacillus strain degrading long-chain n-alkanes. Extremophiles10:347–356 [CrossRef][PubMed]
    [Google Scholar]
  101. Weiss-Penzias P., Jaffe D. A., Swartzendruber P., Dennison J. B., Chand D., Hafner W., Prestbo E.. ( 2006;). Observations of Asian air pollution in the free troposphere at Mount Bachelor Observatory during the spring of 2004. J Geophys Res111:D10304 [CrossRef]
    [Google Scholar]
  102. Wiegand S., Rabausch U., Chow J., Daniel R., Streit W. R., Liesegang H.. ( 2013;). Complete genome sequence of Geobacillus sp. strain GHH01, a thermophilic lipase-secreting bacterium. Genome Announc1:e0009213[PubMed][CrossRef]
    [Google Scholar]
  103. Womack A. M., Bohannan B. J., Green J. L.. ( 2010;). Biodiversity and biogeography of the atmosphere. Philos Trans R Soc Lond B Biol Sci365:3645–3653 [CrossRef][PubMed]
    [Google Scholar]
  104. Yamaguchi N., Ichijo T., Sakotani A., Baba T., Nasu M.. ( 2012;). Global dispersion of bacterial cells on Asian dust. Sci Rep2:525 [CrossRef][PubMed]
    [Google Scholar]
  105. Zeigler D. R.. ( 2005;). Application of a recN sequence similarity analysis to the identification of species within the bacterial genus Geobacillus . Int J Syst Evol Microbiol55:1171–1179 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.071696-0
Loading
/content/journal/micro/10.1099/mic.0.071696-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error