Pyrosequencing-derived bacterial, archaeal, and fungal diversity of spacecraft hardware destined for mars

Applied and Environmental Microbiology

Volumn 78, Issue 16, 2012, Pages 5912-5922

  La Duc, Myron T ^a   Vaishampayan, Parag ^a   Nilsson, Henrik R ^b   Torok, Tamas ^c   Venkateswaran, Kasthuri ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; ACTINOBACTERIA; ARCHAEA; ARCHAEAL; BACTERIAL COMMUNITY; BACTERIAL LINEAGES; BIOINFORMATIC ANALYSIS; CLEANING PROTOCOLS; CO-LOCATED; FIRMICUTES; FUNGAL DIVERSITY; GENOMIC DNA; GROUND SUPPORT EQUIPMENT; HIGH-QUALITY SEQUENCES; INTERNAL TRANSCRIBED SPACERS; LONG JOURNEY; OPERATIONAL TAXONOMIC UNITS; PCR AMPLIFICATION; PROTEOBACTERIA; PYROSEQUENCING; SAMPLE SETS; SPACECRAFT SURFACES; SURFACE SAMPLE;

BACTERIA; BIOINFORMATICS; CLEAN ROOMS; CLEANING; DNA SEQUENCES; FLOORS; FUNGI; GENES; HARDWARE; LABORATORIES; NASA; POLYMERASE CHAIN REACTION; RNA;

SPACECRAFT EQUIPMENT;

ABUNDANCE; BACTERIUM; BIOINFORMATICS; FUNGUS; GENOMICS; HARDWARE; MARS; MICROBIAL COMMUNITY; POLYMERASE CHAIN REACTION; PROKARYOTE; QUALITY CONTROL; SPACECRAFT; SPECIES DIVERSITY;

ARCHAEON; ARTICLE; ASTRONOMY; BACTERIUM; BIODIVERSITY; BIOLOGY; CLASSIFICATION; DNA SEQUENCE; FUNGUS; GENETICS; GOVERNMENT; ISOLATION AND PURIFICATION; MICROBIOLOGY; POLYMERASE CHAIN REACTION; SPACE FLIGHT; UNITED STATES;

ARCHAEA; BACTERIA; BIODIVERSITY; COMPUTATIONAL BIOLOGY; ENVIRONMENTAL MICROBIOLOGY; FUNGI; MARS; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SPACECRAFT; UNITED STATES; UNITED STATES NATIONAL AERONAUTICS AND SPACE ADMINISTRATION;

ACIDOBACTERIA; ACTINOBACTERIA; ARCHAEA; BACTERIA (MICROORGANISMS); DEINOCOCCI; FIRMICUTES; FUNGI; PROTEOBACTERIA;

EID: 84866172403     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01435-12     Document Type: Article

References (62)

1. Abarenkov K, et al. 2010. The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytol. 186:281-285.
2. Amend AS, Seifert KA, Samson R, Bruns TD. 2010. Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proc. Natl. Acad. Sci. U. S. A. 107:13748-13753.
3. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. 2008. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumar-chaeota. Nat. Rev. Microbiol. 6:245-252.
4. Cooper M, et al. 2011. Comparison of innovative molecular approaches and standard spore assays for assessment of surface cleanliness. Appl. Environ. Microbiol. 77:5438-5444.
5. Cordeiro RA, et al. 2010. Isolation of pathogenic yeasts in the air from hospital environments in the city of Fortaleza, northeast Brazil. Braz. J. Infect. Dis. 14:30-34.
6. COSPAR. 2002. Planetary protection policy, October 2002, as amended March 2008. COSPAR, Houston, TX.
7. Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G. 2004. Myco-Bank: an online initiative to launch mycology into the 21st century. Stud. Mycol. 50:19-22.
8. Daly MJ, et al. 2004. Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:1025-1028.
9. Dighton J, Tugay T, Zhdanova N. 2008. Fungi and ionizing radiation from radionuclides. FEMS Microbiol. Lett. 281:109-120.
10. Dowd SE, et al. 2008. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol. 8:43. doi:10.1186/1471-2180-8-43.
11. Ekhaise FO, Ighosewe OU, Ajakpovi OD. 2008. Hospital indoor airborne microflora in private and government owned hospitals in Benin City, Nigeria. World J. Med. Sci. 3:19-23.
12. Favero MS. 1971. Microbiologic assay of space hardware. Environ. Biol. Med. 1:27-36.
13. 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 10:325-335.
14. Good IJ. 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40:237-264.
15. Gtari M, et al. 2012. Contrasted resistance of stone-dwelling Geodermatophilaceae species to stresses known to give rise to reactive oxygen species. FEMS Microbiol. Ecol. 80:566-577.
16. Hartmann M, et al. Significant and persistent impact of timber harvesting on soil microbial communities in northern coniferous forests. ISME J., in press.
17. Hazen TC, et al. 2010. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330:204-208.
18. Huse SM, Welch DM, Morrison HG, Sogin ML. 2010. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Envi- ron. Microbiol. 12:1889-1898.
19. Jacobson ES. 2000. Pathogenic roles for fungal melanins. Clin. Microbiol. Rev. 13:708-717.
20. Karsch-Mizrachi I, Nakamura Y, Cochrane G. 2012. The international nucleotide sequence database collaboration. Nucleic Acids Res. 40:D33-D37.
21. Kim KY, Kim YS, Kim D. 2010. Distribution characteristics of airborne bacteria and fungi in the general hospitals of Korea. Ind. Health 48:236-243.
22. 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. 61:1246-1252.
23. Krasnopolsky VA. 2006. Some problems related to the origin of methane on Mars. Icarus 180:359-367.
24. Kwan K, et al. 2011. Evaluation of procedures for the collection, processing, and analysis of biomolecules from low-biomass surfaces. Appl. Environ. Microbiol. 77:2943-2953.
25. La Duc MT, et al. 2007. Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean-room environments. Appl. Environ. Microbiol. 73:2600-2611.
26. La Duc MT, Kern RG, Venkateswaran K. 2004. Microbial monitoring of spacecraft and associated environments. Microb. Ecol. 47:150-158.
27. La Duc MT, Nicholson W, Kern R, Venkateswaran K. 2003. Microbial characterization of the Mars Odyssey spacecraft and its encapsulation facility. Environ. Microbiol. 5:977-985.
28. La Duc MT, et al. 2009. Comprehensive census of bacteria in clean rooms by using DNA microarray and cloning methods. Appl. Environ. Microbiol. 75:6559-6567.
29. 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 Methods Autom. Microbiol. 17:350-368. doi:10.1111/j.1745-4581.2009.00153.x.
30. Lopolito P, Bartnett C, Polarine J. 2007. Control strategies for fungal contamination in cleanrooms. Control. Environ. 372:1-5. http://www.cemag.us/article/control-strategies-fungal-contamination-cleanrooms?page=0,4.
31. Margulies M, et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-380.
32. McDonald D, et al. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6:610-618.
33. 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. 56:40-47.
34. Moissl C, Bruckner J, Venkateswaran K. 2008. Archaeal diversity analysis of spacecraft assembly facilities. ISME J. 2:115-119.
35. 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. 61:509-521.
36. Mugambi GK, Huhndorf SM. 2009. Molecular phylogenetics of Pleosporales: Melanommataceae and Lophiostomataceae re-circumscribed (Pleosporomycetidae, Dothideomycetes, Ascomycota). Stud. Mycol. 64: 103-121S104. doi:10.3114/sim.2009.64.05.
37. Nagano Y, et al. 2009. Identification of airborne bacterial and fungal species in the clinical microbiology laboratory of a university teaching hospital employing ribosomal DNA (rDNA) PCR and gene sequencing techniques. Int. J. Environ. Health Res. 19:187-199.
38. Neefs JM, Van de Peer Y, Hendriks L, De Wachter R. 1990. Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res. 18(Suppl): 2237-2317.
39. Newcombe DA, et al. 2005. Survival of spacecraft-associated microorganisms under simulated Martian UV irradiation. Appl. Environ. Micro- biol. 71:8147-8156.
40. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH. 2008. Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol. Bioinform. Online 4:193-201.
41. Nilsson RH, et al. 2010. An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high- throughput community assays and molecular ecology. Fungal Ecol. 3:284-287.
42. Onofri S, et al. 2012. Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology 12:508-516.
43. Osman S, et al. 2008. Effect of shadowing on the survival of bacteria to conditions simulating Martian atmosphere and UV radiation. Appl. Environ. Microbiol. 74:959-970.
44. Pace NR. 1997. A molecular view of microbial diversity and the biosphere. Science 276:734-740.
45. Page RD. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
46. Pantoja LD, et al. 2009. Ants (Hymenoptera: Formicidae) as carriers of fungi in hospital environments: an emphasis on the genera Tapinoma and Pheidole. J. Med. Entomol. 46:895-899.
47. Puleo JR, et al. 1977. Microbiological profiles of the Viking spacecraft. Appl. Environ. Microbiol. 33:379-384.
48. Saadoun I, Al Tayyar IA, Elnasser Z. 2008. Concentrations of airborne fungal contaminations in the medical surgery operation theaters (OT) of different hospitals in northern Jordan. Jordan J. Biol. Sci. 1:181-184.
49. Satoh K, et al. 2011. Microbe-I: fungal biota analyses of the Japanese experimental module KIBO of the International Space Station before launch and after being in orbit for about 460 days. Microbiol. Immunol. 55:823-829.
50. Schloss PD, Gevers D, Westcott SL. 2011. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310. doi:10.1371/journal.pone.0027310.
51. Schloss PD, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
52. Selbmann L, de Hoog GS, Mazzaglia A, Friedmann EI, Onofri S. 2005. Fungi at the edge of life: cryptoendolithic black fungi from Antarctic des- erts. Stud. Mycol. 51:1-32.
53. Sogin ML, et al. 2006. Microbial diversity in the deep sea and the under-explored "rare biosphere". Proc. Natl. Acad. Sci. U. S. A. 103:12115-12120.
54. Tedersoo L, et al. 2010. 454 pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol. 188:291-301.
55. Utescher CLDA, Franzolin MR, Trabulsi LR, Gambale V. 2007. Micro-biological monitoring of clean rooms in development of vaccines. Braz. J. Microbiol. 38:710-716.
56. 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 10:499-508.
57. 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 12:487-497. http://online.liebertpub.com /doi/pdfplus/10.1089/ast.2011.0738.
58. Vaishampayan P, et al. Deinococcus phoenicis sp. nov., an extreme ionizing radiation resistant bacterium isolated from the Phoenix Lander assembly facility. Int. J. Syst. Evol. Microbiol., in press.
59. Werner JJ, et al. 2012. Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys. ISME J. 6:94-103.
60. Zhdanova NN, et al. 1991. The interaction of soil micromycetes with "hot" particles in a model system. Mikrobiol. Zh. 53:9-17. (In Russian.)
61. Zhdanova NN, Zakharchenko VA, Haselwandter K. 2005. Radionuclides and fungal communities, p 759-768. In Dighton J, White JF, Oudemans P (ed), The fungal community: its organization and role in the ecosystem. CRC Press, Baton Rouge, LA.
62. Zhdanova NN, Zakharchenko VA, Vember VV, Nakonechnaya LT. 2000. Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol. Res. 104:1421-1426.