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Volume 160, Issue 1

The paradox: why is a thermophilic bacterial genus so prevalent on a mesophilic planet? Free

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.

  • Published Online:
Funding
This study was supported by the:
  • National Science Foundation (Award 0234214)
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2014-01-01
2024-04-19
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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 Res 163:13–20 [View Article][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 [View Article][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 Res 4:1–6[PubMed]
     [Google Scholar]
  4. Ariatti A., Comtois P. ( 1993). Louis Pasteur: the first experimental aerobiologist. Aerobiologia 9:5–14 [View Article]
     [Google Scholar]
  5. Bartholomew J. W., Paik G. ( 1966). Isolation and identification of obligate thermophilic sporeforming bacilli from ocean basin cores. J Bacteriol 92:635–638[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. Microbiology 159:757–770 [View Article][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 Bacteriol 47:1246–1248 [View Article][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 Bioinformatics 10:154 [View Article][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 Microbiol 77:6350–6356 [View Article][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 A 104:299–304 [View Article][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 Phys 9:9281–9297 [View Article]
     [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 Phys 9:9263–9280 [View Article]
     [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 Biotechnol 17:1262–1270[PubMed]
     [Google Scholar]
  14. Cebrian J. ( 1999). Patterns in the fate of production in plant communities. Am Nat 154:449–468 [View Article][PubMed]
     [Google Scholar]
  15. Commichau F. M., Pietack N., Stülke J. ( 2013). Essential genes in Bacillus subtilis: a re-evaluation after ten years. Mol Biosyst 9:1068–1075 [View Article][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 Eng 11:398–408 [View Article][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 Interface 4:183–191 [View Article][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 Microbiol 30:152–164 [View Article][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 A 110:2575–2580 [View Article][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. Extremophiles 10:321–326 [View Article][PubMed]
     [Google Scholar]
  21. Donk P. J. ( 1920). A highly resistant thermophilic organism. J Bacteriol 5:373–374[PubMed]
     [Google Scholar]
  22. Driks A. ( 2002). Maximum shields: the assembly and function of the bacterial spore coat. Trends Microbiol 10:251–254 [View Article][PubMed]
     [Google Scholar]
  23. Fields M. L., Chen Lee P. P. ( 1974). Bacillus stearothermophilus in soils of Iceland. Appl Microbiol 28:638–640[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 Microbiol 51:2063–2071 [View Article][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 Dev 19:2236–2244 [View Article][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 Bacteriol 187:1357–1368 [View Article][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 Microbiol 14:2870–2890 [View Article][PubMed]
     [Google Scholar]
  28. Gilbert H. J. ( 2010). The biochemistry and structural biology of plant cell wall deconstruction. Plant Physiol 153:444–455 [View Article][PubMed]
     [Google Scholar]
  29. Griffin D. W. ( 2007). Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin Microbiol Rev 20:459–477 [View Article][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. Aerobiologia 17:203–213 [View Article]
     [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. Aerobiologia 19:143–157 [View Article]
     [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. Aerobiologia 22:211–226 [View Article]
     [Google Scholar]
  33. Hondoh H., Kuriki T., Matsuura Y. ( 2003). Three-dimensional structure and substrate binding of Bacillus stearothermophilus neopullulanase. J Mol Biol 326:177–188 [View Article][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. Aerobiologia 23:291–298 [View Article]
     [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 A 104:14401–14405 [View Article][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 Trans 35:1610–1615 [View Article][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 Bioeng 91:64–70[PubMed] [CrossRef]
     [Google Scholar]
  38. Kellogg C. A., Griffin D. W. ( 2006). Aerobiology and the global transport of desert dust. Trends Ecol Evol 21:638–644 [View Article][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. Microbiology 140:2513–2529 [View Article][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 Microbiol 59:1725–1730[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 Microbiol 69:644–648 [View Article][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 Microbiol 78:5077–5082 [View Article][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 Bacteriol 175:6441–6450[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 Microbiol 155:283–289 [View Article][PubMed]
     [Google Scholar]
  45. Lambert R. J. ( 2003). A model for the thermal inactivation of micro-organisms. J Appl Microbiol 95:500–507 [View Article][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 Microbiol 108:325–340 [View Article][PubMed]
     [Google Scholar]
  47. Lindahl T. ( 1993). Instability and decay of the primary structure of DNA. Nature 362:709–715 [View Article][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 Microbiol 53:163–166 [View Article][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 Res 40:Database issueD1278–D1287 [View Article][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 Microbiol 4:595–602 [View Article][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 Biotechnol 78:841–852 [View Article][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. Extremophiles 4:365–371 [View Article][PubMed]
     [Google Scholar]
  53. Marquis R. E., Bender G. R. ( 1985). Mineralization and heat resistance of bacterial spores. J Bacteriol 161:789–791[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 ONE 8:e61928 [View Article][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 Microbiol 24:572–587 [View Article][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. Biodegradation 17:105–111 [View Article][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; [View Article]
     [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 Bacteriol 190:1134–1140 [View Article][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 Technol 59:64–86[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 Bacteriol 194:1239 [View Article][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 Microbiol 51:433–446[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 Biosph 33:621–631 [View Article][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 Rev 64:548–572 [View Article][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 Sci 39:314–325 [View Article][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 Microbiol 68:2081–2084 [View Article][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 Microbiol 10:94 [View Article][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 Bioeng 95:84–95 [View Article][PubMed]
     [Google Scholar]
  68. Perfumo A., Marchant R. ( 2010). Global transport of thermophilic bacteria in atmospheric dust. Environ Microbiol Rep 2:333–339 [View Article][PubMed]
     [Google Scholar]
  69. Perfumo A., Banat I. M., Marchant R., Vezzulli L. ( 2007). Thermally enhanced approaches for bioremediation of hydrocarbon-contaminated soils. Chemosphere 66:179–184 [View Article][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 Microbiol 66:930–936 [View Article][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 Technol 31:957–966 [View Article][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 Trans 32:209–213 [View Article][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 Biotechnol 36:585–598 [View Article][PubMed]
     [Google Scholar]
  74. Reanprayoon P., Yoonaiwong W. ( 2012). Airborne concentrations of bacteria and fungi in Thailand border market. Aerobiologia 28:49–60 [View Article]
     [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 Overview 1:1
     [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 Microbiol 85:45–61 [View Article][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 Microbiol 96:263–272 [View Article][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 Microbiol 53:349–410
     [Google Scholar]
  79. Sadaie Y., Nakadate H., Fukui R., Yee L. M., Asai K. ( 2008). Glucomannan utilization operon of Bacillus subtilis . FEMS Microbiol Lett 279:103–109 [View Article][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 Lett 215:163–168 [View Article][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 ONE 6:e20683 [View Article][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 Microbiol 78:7090–7097 [View Article][PubMed]
     [Google Scholar]
  83. Setlow P. ( 2006). Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol 101:514–525 [View Article][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 Microbiol 155:263–268 [View Article][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 Ecol 34:167–177 [View Article][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 Bacteriol 181:3695–3704[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 Bacteriol 193:2838–2850 [View Article][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 A 110:E2084 [View Article][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 Ecol 64:973–985 [View Article][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 Microbiol 79:1134–1139 [View Article][PubMed]
     [Google Scholar]
  91. Strom P. F. ( 1985). Effect of temperature on bacterial species diversity in thermophilic solid-waste composting. Appl Environ Microbiol 50:899–905[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 Microbiol 77:4744–4753 [View Article][PubMed]
     [Google Scholar]
  93. Tabachnikov O., Shoham Y. ( 2013). Functional characterization of the galactan utilization system of Geobacillus stearothermophilus . FEBS J 280:950–964[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 Bioeng 101:42–50 [View Article][PubMed]
     [Google Scholar]
  95. Takamatsu H., Watabe K. ( 2002). Assembly and genetics of spore protective structures. Cell Mol Life Sci 59:434–444 [View Article][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. Extremophiles 8:351–356 [View Article][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 Biotechnol 27:398–405 [View Article][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 A 102:13950–13955 [View Article][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. Aerobiologia 9:69–74 [View Article]
     [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. Extremophiles 10:347–356 [View Article][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 Res 111:D10304 [View Article]
     [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 Announc 1: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 Sci 365:3645–3653 [View Article][PubMed]
     [Google Scholar]
  104. Yamaguchi N., Ichijo T., Sakotani A., Baba T., Nasu M. ( 2012). Global dispersion of bacterial cells on Asian dust. Sci Rep 2:525 [View Article][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 Microbiol 55:1171–1179 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.071696-0
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The Geobacillus paradox: why is a thermophilic bacterial genus so prevalent on a mesophilic planet?
Microbiology 160, 1 (2014); https://doi.org/10.1099/mic.0.071696-0
/content/journal/micro/10.1099/mic.0.071696-0
/content/journal/micro/10.1099/mic.0.071696-0
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