1887

Chapter 4.3.3 : Microbial Life in Extreme Low-Biomass Environments: A Molecular Approach

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $30.00

Preview this chapter:
Zoom in
Zoomout

Microbial Life in Extreme Low-Biomass Environments: A Molecular Approach, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818821/9781555818821.ch4.3.3-1.gif /docserver/preview/fulltext/10.1128/9781555818821/9781555818821.ch4.3.3-2.gif

Abstract:

The capability to (1) systematically collect, process, and archive nucleic acids from "extremely low-biomass" spacecraft-related environments, and (2) effectively assess the diversity of microorganisms present on spacecraft and associated cleanroom surfaces was developed, and validated. This capability enabled generation of the most comprehensive (bacterial, archaeal, and fungal) assessment of spacecraft-associated biodiversity to date. The capability to provide a passenger list of the microorganisms associated with flight hardware developed and validated in this study bridges a significant gap in technology and dramatically increases NASA's ability to explore and verify the scientific findings of both in-situ life detection and sample-return missions.

Although there is a growing understanding of the biodiversity associated with low biomass surfaces, it remains challenging to provide a comprehensive inventory of microbes present. In this study three molecular approaches were attempted: conventional cloning techniques, PhyloChip DNA microarrays, and 454 tag-encoded pyrosequencing, together with a methodology to systematically collect, process, and archive nucleic acids, to assess the phylogenetic breadth of microorganisms present on spacecraft and associated surfaces. The analysis methods yielded very different results; traditional approaches provided the least comprehensive assessment of microbial diversity, while PhlyoChip and pyrosequencing detected more diverse microbial populations. The findings of this pioneering study provided new and important insights into the benefits and limitations of modern molecular approaches for assessing the microbial diversity associated with samples extremely low in total biomass. These are of particular relevance to current and future NASA endeavors, as well as homeland security, medical, pharmaceutical, and semiconductor applications.

Citation: Venkateswaran K, La Duc M, Vaishampayan P, Spry J. 2016. Microbial Life in Extreme Low-Biomass Environments: A Molecular Approach, p 4.3.3-1-4.3.3-11. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.3
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Electron micrographs of exosporium/extraneous layer (EX/EL)-bearing spores. 1, 2: (no EX/EL–shown for comparative purposes); 3: (EX+); 4: (EX+) 5, 6: (EL+) 7, 8: (EL+). doi:10.1128/9781555818821.ch4.3.3.f1

Citation: Venkateswaran K, La Duc M, Vaishampayan P, Spry J. 2016. Microbial Life in Extreme Low-Biomass Environments: A Molecular Approach, p 4.3.3-1-4.3.3-11. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.3
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818821.ch4.3.3
1. NASA 2010. Handbook for the microbiological examination of space hardware, NASA-HDBK-6022. National Aeronautics and Space Administration, Washington, DC.
2. Venkateswaran K, La Duc MT, Vaishampayan P. 2012. Genetic inventory task: final report, JPL Publication 12–12, p. 1117, vol. 1. Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA.
3. Kirschner LE, Puleo JR. 1979. Wipe-rinse technique for quantitating microbial contamination on large surfaces. Appl Environ Microbiol 38:466470.[PubMed]
4. Brown LE, Hannah DM, Milner AM. 2007. Vulnerability of alpine stream biodiversity to shrinking glaciers and snowpacks. Glob Chang Biol 13:958966.[CrossRef]
5. Vesley D, Keenan KM, Halbert MM. 1966. Effect of time and temperature in assessing microbial contamination on flat surfaces. Appl Environ Microbiol 14:203205.
6. Amann RI, Ludwig W, Schleifer KH. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143169.[PubMed]
7. Kaprelyants AS, Gottschal JC, Kell DB. 1993. Dormancy in non-sporulating bacteria. FEMS Microbiol Rev 10:271285.[PubMed][CrossRef]
8. Oliver JD. 2010. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415425.[PubMed][CrossRef]
9. Kell DB, Kaprelyants AS, Weichart DH, Harwood CR, Barer MR. 1998. Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Ant Van Leeuw 73:169187.[CrossRef]
10. Wilson KH, Wilson WJ, Radosevich JL, DeSantis TZ, Viswanathan VS, Kuczmarski TA, Andersen GL. 2002. High-density microarray of small-subunit ribosomal DNA probes. Appl Environ Microbiol 68:25352541.[PubMed][CrossRef]
11. Vaishampayan P, Osman S, Andersen G, Venkateswaran K. 2010. High-density 16S microarray and clone library-based microbial community composition of the Phoenix spacecraft assembly clean room. Astrobiology 10:499508.[PubMed][CrossRef]
12. Hugenholtz P. 2002. Exploring prokaryotic diversity in the genomic era. Genome Biol 3:reviews0003.00010003.0008.[CrossRef]
13. Breitkopf C, Hammel D, Scheld HH, Peters G, Becker K. 2005. Impact of a molecular approach to improve the microbiological diagnosis of infective heart valve endocarditis. Circulation 111:14151421.[PubMed][CrossRef]
14. Girones R, Ferrus MA, Alonso JL, Rodriguez-Manzano J, Calgua B, Correa Ade A, Hundesa A, Carratala A, Bofill-Mas S. 2010. Molecular detection of pathogens in water—the pros and cons of molecular techniques. Water Res 44:43254339.[PubMed][CrossRef]
15. Grindberg RV, Ishoey T, Brinza D, Esquenazi E, Coates RC, Liu WT, Gerwick L, Dorrestein PC, Pevzner P, Lasken R, Gerwick WH. 2011. Single cell genome amplification accelerates identification of the apratoxin biosynthetic pathway from a complex microbial assemblage. PLoS One 6:e18565.[PubMed][CrossRef]
16. Buttner MP, Cruz P, Stetzenbach LD, Klima-Comba AK, Stevens VL, Cronin TD. 2004. Determination of the efficacy of two building decontamination strategies by surface sampling with culture and quantitative PCR analysis. Appl Environ Microbiol 70:47404747.[PubMed][CrossRef]
17. Holman HY, Miles R, Hao Z, Wozei E, Anderson LM, Yang H. 2009. Real-time chemical imaging of bacterial activity in biofilms using open-channel microfluidics and synchrotron FTIR spectromicroscopy. Anal Chem 81:85648570.[PubMed][CrossRef]
18. Rose L, Jensen B, Peterson A, Banerjee SN, Srduino MJ. 2004. Swab materials and Bacillus anthracis spore recovery from nonporous surfaces. Emerg Infect Dis 10:10231029.[PubMed][CrossRef]
19. Buttner MP, Cruz P, Stetzenbach LD, Klima-Comba AK, Stevens VL, Emanuel PA. 2004. Evaluation of the Biological Sampling Kit (BiSKit) for large-area surface sampling. Appl Environ Microbiol 70:70407045.[PubMed][CrossRef]
20. Da Silva SM, Filliben JJ, Morrow JB. 2011. Parameters affecting spore recovery from wipes used in biological surface sampling. Appl Environ Microbiol 77:23742380.[PubMed][CrossRef]
21. Probst A, Facius R, Wirth R, Moissl-Eichinger C. 2010. Validation of a nylon-flocked-swab protocol for efficient recovery of bacterial spores from smooth and rough surfaces. Appl Environ Microbiol 76:51485158.[PubMed][CrossRef]
22. La Duc MT, Osman S, Venkateswaran K. 2009. Comparative analysis of methods for the purification of DNA from low-biomass samples based on total yield and conserved microbial diversity. J Rapid Meth Autom Microbiol 17:350368.[CrossRef]
23. Buttner MP, Cruz P, Stetzenbach LD, Cronin T. 2007. Evaluation of two surface sampling methods for detection of Erwinia herbicola on a variety of materials by culture and quantitative PCR. Appl Environ Microbiol 73:35053510.[PubMed][CrossRef]
24. Gauthier DT, Reece KS, Xiao J, Rhodes MW, Kator HI, Latour RJ, Bonzek CF, Hoenig JM, Vogelbein WK. 2010. Quantitative PCR assay for Mycobacterium pseudoshottsii and Mycobacterium shottsii and application to environmental samples and fishes from the Chesapeake Bay. Appl Environ Microbiol 76:61716179.[PubMed][CrossRef]
25. Garcia SM, Rosenberg AA. 2010. Food security and marine capture fisheries: characteristics, trends, drivers and future perspectives. Phil Trans R Soc Lond B Biol Sci 365:28692880.[CrossRef]
26. Strobel GA, Kluck K, Hess WM, Sears J, Ezra D, Vargas PN. 2007. Muscodor albus E-6, an endophyte of Guazuma ulmifolia making volatile antibiotics: isolation, characterization and experimental establishment in the host plant. Microbiology 153:26132620.[PubMed][CrossRef]
27. Kwan K, Cooper M, La Duc MT, Vaishampayan P, Stam C, Benardini JN, Scalzi G, Moissl-Eichinger C, Venkateswaran K. 2011. Evaluation of procedures for the collection, processing, and analysis of biomolecules from low-biomass surfaces. Appl Environ Microbiol 77:29432953.[PubMed][CrossRef]
28. Bargoma E, La Duc MT, Kwan K, Vaishampayan P, Venkateswaran K. 2013. Differential recovery of phylogenetically disparate microbes from spacecraft-qualified metal surfaces. Astrobiology 13:189202.[PubMed][CrossRef]
29. 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 73:26002611.[PubMed][CrossRef]
30. Ghosh S, Osman S, Vaishampayan P, Venkateswaran K. 2010. Recurrent isolation of extremotolerant bacteria from the clean room where Phoenix spacecraft components were assembled. Astrobiology 10:325335.[PubMed][CrossRef]
31. DeAngelis KM, Wu CH, Beller HR, Brodie EL, Chakraborty R, DeSantis TZ, Fortney JL, Hazen TC, Osman SR, Singer ME, Tom LM, Andersen GL. 2011. PCR amplification-independent methods for detection of microbial communities by the high-density microarray PhyloChip. Appl Environ Microbiol 77:63136322.[PubMed][CrossRef]
32. Pace NR. 1997. A molecular view of microbial diversity and the biosphere. Science 276:734740.[PubMed][CrossRef]
33. La Duc MT, Osman S, Vaishampayan P, Piceno Y, Andersen G, Spry JA, Venkateswaran K. 2009. Comprehensive census of bacteria in clean rooms by using DNA microarray and cloning methods. Appl Environ Microbiol 75:65596567.[PubMed][CrossRef]
34. Brodie EL, DeSantis TZ, Joyner DC, Baek SM, Larsen JT, Andersen GL, Hazen TC, Richardson PM, Herman DJ, Tokunaga TK, Wan JM, Firestone MK. 2006. Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 72:62886298.[PubMed][CrossRef]
35. DeSantis TZ, Brodie EL, Moberg JP, Zubieta IX, Piceno YM, Andersen GL. 2007. High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment. Microb Ecol 53:371383.[PubMed][CrossRef]
36. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, Piceno YM, DeSantis TZ, Andersen GL, Bakker PA, Raaijmakers JM. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:10971100.[PubMed][CrossRef]
37. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ. 2006. Microbial diversity in the deep sea and the underexplored “rare biosphere.” Proc Natl Acad Sci USA 103:1211512120.[PubMed][CrossRef]
38. La Duc MT, Nicholson W, Kern R, Venkateswaran K. 2003. Microbial characterization of the Mars Odyssey spacecraft and its encapsulation facility. Environ Microbiol 5:977985.[PubMed][CrossRef]
39. Venkateswaran K, Kempf M, Chen F, Satomi M, Nicholson W, Kern R. 2003. Bacillus nealsonii sp. nov., isolated from a spacecraft-assembly facility, whose spores are gamma-radiation resistant. Int J Syst Evol Microbiol 53:165172.[PubMed][CrossRef]
40. La Duc MT, Satomi M, Venkateswaran K. 2004. Bacillus odysseyi sp. nov., a round-spore-forming bacillus isolated from the Mars Odyssey spacecraft. Int J Syst Evol Microbiol 54:195201.[PubMed][CrossRef]
41. Satomi M, La Duc MT, Venkateswaran K. 2006. Bacillus safensis sp. nov., isolated from spacecraft and assembly-facility surfaces. Int J Syst Evol Microbiol 56:17351740.[PubMed][CrossRef]
42. Newcombe D, Dekas A, Mayilraj S, Venkateswaran K. 2009. Bacillus canaveralius sp. nov., an alkali-tolerant bacterium isolated from a spacecraft assembly facility. Int J Syst Evol Microbiol 59:20152019.[PubMed][CrossRef]
43. Vaishampayan P, Probst A, Krishnamurthi S, Ghosh S, Osman S, McDowall A, Ruckmani A, Mayilraj S, Venkateswaran K. 2010. Bacillus horneckiae sp. nov., isolated from a spacecraft-assembly clean room. Int J Syst Evol Microbiol 60:10311037.[PubMed][CrossRef]
44. Osman S, Satomi M, Venkateswaran K. 2006. Paenibacillus pasadenensis sp. nov. and Paenibacillus barengoltzii sp. nov., isolated from a spacecraft assembly facility. Int J Syst Evol Microbiol 56:15091514.[PubMed][CrossRef]
45. Benardini JN, Vaishampayan PA, Schwendner P, Swanner E, Fukui Y, Osman S, Satomi M, Venkateswaran K. 2011. Paenibacillus phoenicis sp. nov., isolated from the Phoenix lander assembly facility and a subsurface molybdenum mine. Int J Syst Evol Microbiol 61:13381343.[PubMed][CrossRef]
46. Vaishampayan P, Miyashita M, Ohnishi A, Satomi M, Rooney A, La Duc MT, Venkateswaran K. 2009. Description of Rummeliibacillus stabekisii gen. nov., sp. nov. and reclassification of Bacillus pycnus Nakamura et al. 2002 as Rummeliibacillus pycnus comb. nov. Int J Syst Evol Microbiol 59:10941099.[PubMed][CrossRef]
47. Vaishampayan P, Roberts AH, Augustus A, Schwendner P, Mayilraj S, Salmassi T, Venkateswaran K. 2013. Deinococcus phoenicis sp. nov., an extreme ionizing radiation resistant bacterium isolated from the Phoenix Lander assembly facility. Int J Syst Evol Micriobiol submitted 10.1099/ijs.0.063107-0. http://dx.doi.org/10.1099/ijs.0.063107-
48. Vaishampayan P, Moissl-Eichinger C, Pukall R, Schumann P, Sproer C, Augustus A, Hayden Roberts A, Namba G, Cisneros J, Salmassi T, Venkateswaran K. 2013. Description of Tersicoccus phoenicis gen. nov., sp. nov. isolated from spacecraft assembly clean room environments. Int J Syst Evol Microbiol 63:24632471.[PubMed][CrossRef]
49. Osman S, Moissl C, Hosoya N, Briegel A, Mayilraj S, Satomi M, Venkateswaran K. 2007. Tetrasphaera remsis sp. nov., isolated from the Regenerative Enclosed Life Support Module Simulator (REMS) air system. Int J Syst Evol Microbiol 57:27492753.[PubMed][CrossRef]
50. Kempf MJ, Chen F, Kern R, Venkateswaran K. 2005. Recurrent isolation of hydrogen peroxide–resistant spores of Bacillus pumilus from a spacecraft assembly facility. Astrobiology 5:391405.[PubMed][CrossRef]
51. Link L, Sawyer J, Venkateswaran K, Nicholson W. 2004. Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean spacecraft assembly facility. Microb Ecol 47:159163.[PubMed][CrossRef]
52. Kieft TL,. 2000. Size matters: dwarf cells in soil and subsurface terrestrial environments. In Colwell RR,, Grimes DJ (ed), Nonculturable microorganisms in the environment. ASM Press, Washington, DC.
53. Stackebrandt E, Embley TM,. 2000. Diversity of uncultured microorganisms in the environment, p. 5773. In Colwell RR,, Grimes DJ (ed), Nonculturable microorganisms in the environment, vol. 46. ASM Press, Washington, DC.
54. Moter A, Gobel UB. 2000. Fluorescence in situ hybridization (FISH) for direct visualization of microorganisms. J Microbiol Meth 41:85112.[CrossRef]
55. Mohapatra BR, La Duc MT. 2012. Evaluation of fluorescence in situ hybridization to detect encapsulated Bacillus pumilus SAFR-032 spores released from poly(methylmethacrylate). Microbiol Immunol 56:4047.[PubMed][CrossRef]
56. Puyen ZM, Villagrasa E, Maldonado J, Esteve I, Sole A. 2012. Viability and biomass of Micrococcus luteus DE2008 at different salinity concentrations determined by specific fluorochromes and CLSM-image analysis. Curr Microbiol 64:7580.[PubMed][CrossRef]
57. Mohapatra BR, La Duc MT. 2012. Rapid detection of viable Bacillus pumilus SAFR-032 encapsulated spores using novel propidium monoazide-linked fluorescence in situ hybridization. J Microbiol Meth 90:1519.[CrossRef]
58. La Duc MT, Kern RG, Venkateswaran K. 2004. Microbial monitoring of spacecraft and associated environments. Microb Ecol 47:150158.[PubMed][CrossRef]
59. Venkateswaran K, Hattori N, La Duc MT, Kern R. 2003. ATP as a biomarker of viable microorganisms in clean-room facilities. J Microbiol Meth 52:367377.[CrossRef]
60. van Frankenhuyzen JK, Trevors JT, Lee H, Flemming CA, Habash MB. 2011. Molecular pathogen detection in biosolids with a focus on quantitative PCR using propidium monoazide for viable cell enumeration. J Microbiol Meth 87:263272.[CrossRef]
61. Nocker A, Mazza A, Masson L, Camper AK, Brousseau R. 2009. Selective detection of live bacteria combining propidium monoazide sample treatment with microarray technology. J Microbiol Meth 76:253261.[CrossRef]
62. Vaishampayan P, Probst AJ, La Duc MT, Bargoma E, Benardini JN, Andersen GL, Venkateswaran K. 2013. New perspectives on viable microbial communities in low-biomass cleanroom environments. ISME J 7:312324.[PubMed][CrossRef]
63. Sogin SJ, Sogin ML, Woese CR. 1971. Phylogenetic measurement in procaryotes by primary structural characterization. J Mol Evol 1:173184.[PubMed][CrossRef]
64. Woese CR, Fox GE. 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:50885090.[PubMed][CrossRef]
65. Woese CR, Sogin ML, Sutton LA. 1974. Procaryote phylogeny. I. Concerning the relatedness of Aerobacter aerogenes to Escherichia coli. J Mol Evol 3:293299.[PubMed][CrossRef]
66. Fox GE, Pechman KR, Woese CR. 1977. Comparative cataloging of 16S ribosomal ribonucleic acid: Molecular approach to prokaryotic systematic. Int J Syst Bacteriol 27:4457.[CrossRef]
67. Fox GE, Stackebrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner RS, Magrum LJ, Zablen LB, Blakemore R, Gupta R, Bonen L, Lewis BJ, Stahl DA, Luehrsen KR, Chen KN, Woese CR. 1980. The phylogeny of prokaryotes. Science 209:457463.[PubMed][CrossRef]
68. Woese CR, Stackebrandt E, Macke TJ, Fox GE. 1985. A phylogenetic definition of the major eubacterial taxa. Syst Appl Microbiol 6:143151.[PubMed][CrossRef]
69. Woese CR, Magrum LJ, Fox GE. 1978. Archaebacteria. J Mol Evol 11:245251.[PubMed][CrossRef]
70. Ley RE, Peterson DA, Gordon JI. 2006. An extended view of ourselves: ecological and evolutionary forces that shape microbial diversity and genome content in the human intestine. Cell 124:837848.[PubMed][CrossRef]
71. Moissl C, Osman S, La Duc MT, Dekas A, Brodie E, DeSantis T, Venkateswaran K. 2007. Molecular bacterial community analysis of clean rooms where spacecraft are assembled. FEMS Microbiol Ecol 61:509521.[PubMed][CrossRef]
72. Osman S, Peeters Z, La Duc MT, Mancinelli R, Ehrenfreund P, Venkateswaran K. 2008. Effect of shadowing on survival of bacteria under conditions simulating the Martian atmosphere and UV radiation. Appl Environ Microbiol 74:959970.[PubMed][CrossRef]
73. Gtari M, Essoussi I, Maaoui R, Sghaier H, Boujmil R, Gury J, Pujic P, Brusetti L, Chouaia B, Crotti E, Daffonchio D, Boudabous A, Normand P. 2012. Contrasted resistance of stone-dwelling Geodermatophilaceae species to stresses known to give rise to reactive oxygen species. FEMS Microbiol Ecol 80:566577.[PubMed][CrossRef]
74. Newcombe DA, Schuerger AC, Benardini JN, Dickinson D, Tanner R, Venkateswaran K. 2005. Survival of spacecraft-associated microorganisms under simulated martian UV irradiation. Appl Environ Microbiol 71:81478156.[PubMed][CrossRef]
75. Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Venkateswaran A, Hess M, Omelchenko MV, Kostandarithes HM, Makarova KS, Wackett LP, Fredrickson JK, Ghosal D. 2004. Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:10251028[PubMed][CrossRef]
76. Vaishampayan P, Rabbow E, Horneck G, Venkateswaran K. 2012. Survival of Bacillus pumilus spores for a prolonged period of time in real space conditions. Astrobiology 12:487497.[PubMed][CrossRef]
77. Moissl C, Bruckner JC, Venkateswaran K. 2008. Archaeal diversity analysis of spacecraft assembly clean rooms. ISME J 2:115119.[PubMed][CrossRef]
78. La Duc MT, Vaishampayan P, Nilsson HR, Torok T, Venkateswaran K. 2012. Pyrosequencing-derived bacterial, archaeal, and fungal diversity of spacecraft hardware destined for Mars. Appl Environ Microbiol 78:59125922.[PubMed][CrossRef]
79. Moissl C, La Duc MT, Osman S, Dekas AE, Venkateswaran K. 2007. Molecular bacterial community analysis of clean rooms where spacecraft are assembled. FEMS Microbiol Ecol 61:509521.[PubMed][CrossRef]
80. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. 2008. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245252.[PubMed][CrossRef]
81. Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C. 2011. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108:84208425.[PubMed][CrossRef]
82. Kitamura K, Fujita T, Akada S, Tonouchi A. 2011. Methanobacterium kanagiense sp. nov., a hydrogenotrophic methanogen, isolated from rice-field soil. Int J Syst Evol Microbiol 61:12461252.[PubMed][CrossRef]
83. Probst A, Vaishampayan P, Osman S, Moissl-Eichinger C, Andersen GL, Venkateswaran K. 2010. Diversity of anaerobic microbes in spacecraft assembly clean rooms. Appl Environ Microbiol 76:28372845.[PubMed][CrossRef]
84. Horneck G. 1993. Responses of Bacillus subtilis spores to space environment: results from experiments in space. Orig Life Evol Biosph 23:3752.[PubMed][CrossRef]
85. Horneck G, Klaus DM, Mancinelli RL. 2010. Space microbiology. Microbiol Mol Biol Rev 74:121156.[PubMed][CrossRef]
86. Rettberg P, Eschweiler U, Strauch K, Reitz G, Horneck G, Wanke H, Brack A, Barbier B. 2002. Survival of microorganisms in space protected by meteorite material: results of the experiment “EXOBIOLOGIE” of the PERSEUS mission. Adv Space Res 30:15391545.[PubMed][CrossRef]
87. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548572.[PubMed][CrossRef]
88. Schuerger AC, Mancinelli RL, Kern RG, Rothschild LJ, McKay CP. 2003. Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated Martian environments: implications for the forward contamination of Mars. Icarus 165:253276.[PubMed][CrossRef]
89. Schuerger AC, Richards JT, Newcombe DA, Venkateswaran K. 2006. Rapid inactivation of seven Bacillus spp* under simulated Mars UV irradiation. Icarus 181:5262.[CrossRef]
90. Horneck G, Bucker H, Reitz G. 1994. Long-term survival of bacterial spores in space. Adv Space Res 14:4145.[PubMed][CrossRef]
91. Horneck G, Eschweiler U, Reitz G, Wehner J, Willimek R, Strauch K. 1995. Biological responses to space: results of the experiment “Exobiological Unit” of ERA on EURECA I. Adv Space Res 16:105118.[PubMed][CrossRef]
92. Horneck G, Bucker H, Dose K, Martens KD, Bieger A, Mennigmann HD, Reitz G, Requardt H, Weber P. 1984. Microorganisms and biomolecules in space environment experiment ES 029 on Spacelab-1. Adv Space Res 4:1927.[PubMed][CrossRef]
93. Horneck G, Rettberg P, Reitz G, Wehner J, Eschweiler U, Strauch K, Panitz C, Starke V, Baumstark-Khan C. 2001. Protection of bacterial spores in space, a contribution to the discussion on Panspermia. Orig Life Evol Biosph 31:527547.[PubMed][CrossRef]
94. Tauscher C, Schuerger AC, Nicholson WL. 2006. Survival and germinability of Bacillus subtilis spores exposed to simulated Mars solar radiation: implications for life detection and planetary protection. Astrobiology 6:592605.[PubMed][CrossRef]
95. Moores JE, Smith PH, Tanner R, Schuerger AC, Venkateswaran K. 2007. The shielding effect of small-scale Martian surface geometry on ultraviolet lux. Icarus 192:417433.[CrossRef]

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error