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Applied Microbiology and Biotechnology

, Volume 103, Issue 3, pp 1363–1377 | Cite as

International Space Station conditions alter genomics, proteomics, and metabolomics in Aspergillus nidulans

  • Jillian Romsdahl
  • Adriana Blachowicz
  • Abby J. Chiang
  • Yi-Ming Chiang
  • Sawyer Masonjones
  • Junko Yaegashi
  • Stefanie Countryman
  • Fathi Karouia
  • Markus Kalkum
  • Jason E. Stajich
  • Kasthuri Venkateswaran
  • Clay C. C. WangEmail author
Genomics, transcriptomics, proteomics

Abstract

The first global genomic, proteomic, and secondary metabolomic characterization of the filamentous fungus Aspergillus nidulans following growth onboard the International Space Station (ISS) is reported. The investigation included the A. nidulans wild-type and three mutant strains, two of which were genetically engineered to enhance secondary metabolite production. Whole genome sequencing revealed that ISS conditions altered the A. nidulans genome in specific regions. In strain CW12001, which features overexpression of the secondary metabolite global regulator laeA, ISS conditions induced the loss of the laeA stop codon. Differential expression of proteins involved in stress response, carbohydrate metabolic processes, and secondary metabolite biosynthesis was also observed. ISS conditions significantly decreased prenyl xanthone production in the wild-type strain and increased asperthecin production in LO1362 and CW12001, which are deficient in a major DNA repair mechanism. These data provide valuable insights into the adaptation mechanism of A. nidulans to spacecraft environments.

Keywords

Aspergillus nidulans International Space Station Genomics Proteomics Metabolomics 

Notes

Acknowledgements

Part of the research described in this publication was carried out at the Jet Propulsion Laboratory, California Institute of Technology, under a contract with NASA. We would like to thank astronauts Tim Peake, Tim Kopra, and Jeff Williams for handling the samples aboard the ISS, the Implementation Team at NASA Ames Research Center, and BioServe Space Technologies for coordinating this effort. © 2018 California Institute of Technology. Government sponsorship acknowledged.

Reference herein to any specific commercial product, process, or service by trade name, trademark, manufacturer, or otherwise does not constitute or imply its endorsement by the U.S. Government or the Jet Propulsion Laboratory, California Institute of Technology.

Author contributions

JR drafted the manuscript, contributed to sample processing, and was responsible for data analysis and interpretation. AB contributed to sample processing and data interpretation. AC and MK conducted protein sample processing, LC/MS analyses, and proteome data processing. YC contributed to secondary metabolic analysis and interpretation. SM contributed to variant analysis. JY generated the CW12001 strain. SC was responsible for sample integration into flight hardware. FK was responsible for project implementation and generating metadata from the ISS. JS contributed to genome data processing and variant analysis. KV and CW designed the study, interpreted the data, and drafted the manuscript. All authors read and approved the final manuscript.

Funding

This research was funded by a 2012 Space Biology NNH12ZTT001N grant nos. 19-12829-26 under Task Order NNN13D111T awarded to CW and KV, which also funded JR and AB.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

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

Supplementary material

253_2018_9525_MOESM1_ESM.pdf (35.2 mb)
ESM 1 (PDF 36056 kb)

References

  1. Amaral Zettler LA, Gómez F, Zettler E, Keenan BG, Amils R, Sogin ML (2002) Microbiology: eukaryotic diversity in Spain’s River of Fire. Nature 417:137.  https://doi.org/10.1038/417137a CrossRefGoogle Scholar
  2. Andersen MR, Nielsen JB, Klitgaard A, Petersen LM, Zachariasen M, Hansen TJ, Blicher LH, Gotfredsen CH, Larsen T, Nielsen KF, Mortensen UH (2013) Accurate prediction of secondary metabolite gene clusters in filamentous fungi. Proc Natl Acad Sci 110:E99–E107.  https://doi.org/10.1073/pnas.1205532110 CrossRefGoogle Scholar
  3. Andrews S (2010) FastQC: a quality control tool for high throughput sequence dataGoogle Scholar
  4. Arena C, De Micco V, Macaeva E, Quintens R (2014) Space radiation effects on plant and mammalian cells. Acta Astronaut 104:419–431.  https://doi.org/10.1016/j.actaastro.2014.05.005 CrossRefGoogle Scholar
  5. Arnaud MB, Chibucos MC, Costanzo MC, Crabtree J, Inglis DO, Lotia A, Orvis J, Shah P, Skrzypek MS, Binkley G, Miyasato SR, Wortman JR, Sherlock G (2010) The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res 38:D420–D427.  https://doi.org/10.1093/nar/gkp751 CrossRefGoogle Scholar
  6. Barnard RL, Osborne CA, Firestone MK (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229–2241.  https://doi.org/10.1038/ismej.2013.104 CrossRefGoogle Scholar
  7. Bayram ÖS, Bayram Ö, Valerius O, Park HS, Irniger S, Gerke J, Ni M, Han K-H, Yu J-H, Braus GH (2010) LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet 6:e1001226.  https://doi.org/10.1371/journal.pgen.1001226 CrossRefGoogle Scholar
  8. Benoit MR, Li W, Stodieck LS, Lam KS, Winther CL, Roane TM, Klaus DM (2006) Microbial antibiotic production aboard the International Space Station. Appl Microbiol Biotechnol 70:403–411.  https://doi.org/10.1007/s00253-005-0098-3 CrossRefGoogle Scholar
  9. Bok JW, Keller NP (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3:527–535CrossRefGoogle Scholar
  10. Bok JW, Keller NP (2016) Insight into fungal secondary metabolism from ten years of LaeA research. In: Biochemistry and molecular biology. Springer, Cham, pp 21–29CrossRefGoogle Scholar
  11. Bok JW, Hoffmeister D, Maggio-Hall LA, Murillo R, Glasner JD, Keller NP (2006) Genomic mining for Aspergillus natural products. Chem Biol 13:31–37.  https://doi.org/10.1016/j.chembiol.2005.10.008 CrossRefGoogle Scholar
  12. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120.  https://doi.org/10.1093/bioinformatics/btu170 CrossRefGoogle Scholar
  13. Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32.  https://doi.org/10.1038/nrmicro2916 CrossRefGoogle Scholar
  14. Brown DW, Adams TH, Keller NP (1996a) Aspergillus has distinct fatty acid synthases for primary and secondary metabolism. Proc Natl Acad Sci 93:14873–14877.  https://doi.org/10.1073/pnas.93.25.14873 CrossRefGoogle Scholar
  15. Brown DW, Yu JH, Kelkar HS, Fernandes M, Nesbitt TC, Keller NP, Adams TH, Leonard TJ (1996b) Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc Natl Acad Sci 93:1418–1422.  https://doi.org/10.1073/pnas.93.4.1418 CrossRefGoogle Scholar
  16. Capy P, Gasperi G, Biémont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101–106.  https://doi.org/10.1046/j.1365-2540.2000.00751.x CrossRefGoogle Scholar
  17. Chang P-K, Scharfenstein LL, Ehrlich KC, Wei Q, Bhatnagar D, Ingber BF (2012) Effects of laeA deletion on Aspergillus flavus conidial development and hydrophobicity may contribute to loss of aflatoxin production. Fungal Biol 116:298–307.  https://doi.org/10.1016/j.funbio.2011.12.003 CrossRefGoogle Scholar
  18. Checinska A, Probst AJ, Vaishampayan P, White JR, Kumar D, Stepanov VG, Fox GE, Nilsson HR, Pierson DL, Perry J, Venkateswaran K (2015) Microbiomes of the dust particles collected from the International Space Station and Spacecraft Assembly Facilities. Microbiome 3:50.  https://doi.org/10.1186/s40168-015-0116-3 CrossRefGoogle Scholar
  19. Chiang Y-M, Szewczyk E, Nayak T, Davidson AD, Sanchez JF, Lo H-C, Ho W-Y, Simityan H, Kuo E, Praseuth A, Watanabe K, Oakley BR, Wang CCC (2008) Molecular genetic mining of the Aspergillus secondary metabolome: discovery of the emericellamide biosynthetic pathway. Chem Biol 15:527–532.  https://doi.org/10.1016/j.chembiol.2008.05.010 CrossRefGoogle Scholar
  20. Chiang Y-M, Szewczyk E, Davidson AD, Entwistle R, Keller NP, Wang CCC, Oakley BR (2010) Characterization of the Aspergillus nidulans monodictyphenone gene cluster. Appl Environ Microbiol 76:2067–2074.  https://doi.org/10.1128/AEM.02187-09 CrossRefGoogle Scholar
  21. Council NR (2011) Recapturing a future for space exploration: life and physical sciences research for a new eraGoogle Scholar
  22. de Crecy E, Jaronski S, Lyons B, Lyons TJ, Keyhani NO (2009) Directed evolution of a filamentous fungus for thermotolerance. BMC Biotechnol 9:74.  https://doi.org/10.1186/1472-6750-9-74 CrossRefGoogle Scholar
  23. Dadachova E, Casadevall A (2008) Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr Opin Microbiol 11:525–531.  https://doi.org/10.1016/j.mib.2008.09.013 CrossRefGoogle Scholar
  24. DePristo MA, Banks E, Poplin RE, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas M, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498.  https://doi.org/10.1038/ng.806 CrossRefGoogle Scholar
  25. Fujii K, Kurata H, Odashima S, Hatsuda Y (1976) Tumor induction by a single subcutaneous injection of sterigmatocystin in newborn mice. Cancer Res 36:1615–1618Google Scholar
  26. Galagan JE, Calvo SE, Cuomo C, Ma L-J, Wortman JR, Batzoglou S, Lee S-I, Baştürkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D’Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Peñalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115.  https://doi.org/10.1038/nature04341 CrossRefGoogle Scholar
  27. Gunde-Cimerman N, Ramos J, Plemenitas A (2009) Halotolerant and halophilic fungi. Mycol Res 113:1231–1241.  https://doi.org/10.1016/j.mycres.2009.09.002 CrossRefGoogle Scholar
  28. Guo J, Han N, Zhang Y, Wang H, Zhang X, Su L, Liu C, Li J, Chen C, Liu C (2015) Use of genome sequencing to assess nucleotide structure variation of Staphylococcus aureus strains cultured in spaceflight on Shenzhou-X, under simulated microgravity and on the ground. Microbiol Res 170:61–68.  https://doi.org/10.1016/j.micres.2014.09.001 CrossRefGoogle Scholar
  29. Haas H (2015) Microbial ecology: how to trigger a fungal weapon. eLife 4:e10504.  https://doi.org/10.7554/eLife.10504 CrossRefGoogle Scholar
  30. van Hoof A, Frischmeyer PA, Dietz HC, Parker R (2002) Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295:2262–2264.  https://doi.org/10.1126/science.1067272 CrossRefGoogle Scholar
  31. Horneck G, Baumstark-Khan C, Facius R (2006) Radiation biology. In: Clément G, Slenzka K (eds) Fundamentals of space biology. Springer, New York, pp 291–336CrossRefGoogle Scholar
  32. Horneck G, Klaus DM, Mancinelli RL (2010) Space microbiology. Microbiol Mol Biol Rev 74:121–156.  https://doi.org/10.1128/MMBR.00016-09 CrossRefGoogle Scholar
  33. Huang B, Li D-G, Huang Y, Liu C-T (2018) Effects of spaceflight and simulated microgravity on microbial growth and secondary metabolism. Mil Med Res 5:18.  https://doi.org/10.1186/s40779-018-0162-9 CrossRefGoogle Scholar
  34. Hunter GD, Bailey CR, Arst HN (1992) Expression of a bacterial aspartase gene in Aspergillus nidulans: an efficient system for selecting multicopy transformants. Curr Genet 22:377–383.  https://doi.org/10.1007/BF00352439 CrossRefGoogle Scholar
  35. Jeong H-Y, Chae K-S, Whang SS (2004) Presence of a mannoprotein, MnpAp, in the hyphal cell wall of Aspergillus nidulans. Mycologia 96:52–56.  https://doi.org/10.1080/15572536.2005.11832996 CrossRefGoogle Scholar
  36. Klauer AA, van Hoof A (2012) Degradation of mRNAs that lack a stop codon: a decade of nonstop progress. Wiley Interdiscip Rev RNA 3:649–660.  https://doi.org/10.1002/wrna.1124 CrossRefGoogle Scholar
  37. Knox BP, Blachowicz A, Palmer JM, Romsdahl J, Huttenlocher A, Wang CCC, Keller NP, Venkateswaran K (2016) Characterization of Aspergillus fumigatus isolates from air and surfaces of the International Space Station. mSphere 1:e00227–e00216.  https://doi.org/10.1128/mSphere.00227-16 CrossRefGoogle Scholar
  38. Kosalková K, García-Estrada C, Ullán RV, Godio RP, Feltrer R, Teijeira F, Mauriz E, Martín JF (2009) The global regulator LaeA controls penicillin biosynthesis, pigmentation and sporulation, but not roquefortine C synthesis in Penicillium chrysogenum. Biochimie 91:214–225.  https://doi.org/10.1016/j.biochi.2008.09.004 CrossRefGoogle Scholar
  39. Krappmann S (2007) Gene targeting in filamentous fungi: the benefits of impaired repair. Fungal Biol Rev 21:25–29.  https://doi.org/10.1016/j.fbr.2007.02.004 CrossRefGoogle Scholar
  40. de la Torre Noetzel R, Miller AZ, de la Rosa JM, Pacelli C, Onofri S, García Sancho L, Cubero B, Lorek A, Wolter D, de Vera JP (2018) Cellular responses of the lichen Circinaria gyrosa in Mars-like conditions. Front Microbiol 9.  https://doi.org/10.3389/fmicb.2018.00308
  41. Lam KS, Mamber SW, Pack EJ, Forenza S, Fernandes PB, Klaus DM (1998) The effects of space flight on the production of monorden by Humicola fuscoatra WC5157 in solid-state fermentation. Appl Microbiol Biotechnol 49:579–583CrossRefGoogle Scholar
  42. Lam KS, Gustavson DR, Pirnik DL, Pack E, Bulanhagui C, Mamber SW, Forenza S, Stodieck LS, Klaus DM (2002) The effect of space flight on the production of actinomycin D by Streptomyces plicatus. J Ind Microbiol Biotechnol 29:299–302.  https://doi.org/10.1038/sj.jim.7000312 CrossRefGoogle Scholar
  43. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760.  https://doi.org/10.1093/bioinformatics/btp324 CrossRefGoogle Scholar
  44. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinforma Oxf Engl 25:2078–2079.  https://doi.org/10.1093/bioinformatics/btp352 CrossRefGoogle Scholar
  45. Lo H-C, Entwistle R, Guo C-J, Ahuja M, Szewczyk E, Hung J-H, Chiang Y-M, Oakley BR, Wang CCC (2012) Two separate gene clusters encode the biosynthetic pathway for the meroterpenoids austinol and dehydroaustinol in Aspergillus nidulans. J Am Chem Soc 134:4709–4720.  https://doi.org/10.1021/ja209809t CrossRefGoogle Scholar
  46. López-Archilla AI, Marin I, Amils R (2001) Microbial community composition and ecology of an acidic aquatic environment: the Tinto River. Spain Microb Ecol 41:20–35.  https://doi.org/10.1007/s002480000044 Google Scholar
  47. Lv Y, Lv A, Zhai H, Zhang S, Li L, Cai J, Hu Y (2018) Insight into the global regulation of laeA in Aspergillus flavus based on proteomic profiling. Int J Food Microbiol 284:11–21.  https://doi.org/10.1016/j.ijfoodmicro.2018.06.024 CrossRefGoogle Scholar
  48. MacCabe AP, Orejas M, Tamayo EN, Villanueva A, Ramón D (2002) Improving extracellular production of food-use enzymes from Aspergillus nidulans. J Biotechnol 96:43–54CrossRefGoogle Scholar
  49. Martinez-Lopez R, Monteoliva L, Diez-Orejas R, Nombela C, Gil C (2004) The GPI-anchored protein CaEcm33p is required for cell wall integrity, morphogenesis and virulence in Candida albicans. Microbiology 150:3341–3354.  https://doi.org/10.1099/mic.0.27320-0 CrossRefGoogle Scholar
  50. McCluskey K, Wiest A, Plamann M (2010) The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci 35:119–126.  https://doi.org/10.1007/s12038-010-0014-6 CrossRefGoogle Scholar
  51. Meyer V, Arentshorst M, El-Ghezal A, Drews A-C, Kooistra R, van den Hondel CAMJJ, Ram AFJ (2007) Highly efficient gene targeting in the Aspergillus niger kusA mutant. J Biotechnol 128:770–775.  https://doi.org/10.1016/j.jbiotec.2006.12.021 CrossRefGoogle Scholar
  52. Micco VD, Arena C, Pignalosa D, Durante M (2011) Effects of sparsely and densely ionizing radiation on plants. Radiat Environ Biophys 50:1–19.  https://doi.org/10.1007/s00411-010-0343-8 CrossRefGoogle Scholar
  53. Mora M, Perras A, Alekhova TA, Wink L, Krause R, Aleksandrova A, Novozhilova T, Moissl-Eichinger C (2016) Resilient microorganisms in dust samples of the International Space Station—survival of the adaptation specialists. Microbiome 4:65.  https://doi.org/10.1186/s40168-016-0217-7 CrossRefGoogle Scholar
  54. Nayak T, Szewczyk E, Oakley CE, Osmani A, Ukil L, Murray SL, Hynes MJ, Osmani SA, Oakley BR (2006) A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172:1557–1566.  https://doi.org/10.1534/genetics.105.052563 CrossRefGoogle Scholar
  55. Newman DJ, Cragg GM (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 75:311–335.  https://doi.org/10.1021/np200906s CrossRefGoogle Scholar
  56. Novikova ND (2004) Review of the knowledge of microbial contamination of the Russian manned spacecraft. Microb Ecol 47:127–132.  https://doi.org/10.1007/s00248-003-1055-2 CrossRefGoogle Scholar
  57. Novikova N, De Boever P, Poddubko S, Deshevaya E, Polikarpov N, Rakova N, Coninx I, Mergeay M (2006) Survey of environmental biocontamination on board the International Space Station. Res Microbiol 157:5–12.  https://doi.org/10.1016/j.resmic.2005.07.010 CrossRefGoogle Scholar
  58. Oakley CE, Ahuja M, Sun W-W, Entwistle R, Akashi T, Yaegashi J, Guo C-J, Cerqueira GC, Russo Wortman J, Wang CCC, Chiang Y-M, Oakley BR (2017) Discovery of McrA, a master regulator of Aspergillus secondary metabolism. Mol Microbiol 103:347–365.  https://doi.org/10.1111/mmi.13562 CrossRefGoogle Scholar
  59. Onofri S, Selbmann L, de Hoog GS, Grube M, Barreca D, Ruisi S, Zucconi L (2007) Evolution and adaptation of fungi at boundaries of life. Adv Space Res 40:1657–1664.  https://doi.org/10.1016/j.asr.2007.06.004 CrossRefGoogle Scholar
  60. Onofri S, Barreca D, Selbmann L, Isola D, Rabbow E, Horneck G, de Vera JPP, Hatton J, Zucconi L (2008) Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Martian conditions. Stud Mycol 61:99–109.  https://doi.org/10.3114/sim.2008.61.10 CrossRefGoogle Scholar
  61. Onofri S, Selbmann L, Pacelli C, de Vera JP, Horneck G, Hallsworth JE, Zucconi L (2018a) Integrity of the DNA and cellular ultrastructure of cryptoendolithic fungi in space or Mars conditions: a 1.5-year study at the International Space Station. Life Basel Switz 8:.  https://doi.org/10.3390/life8020023
  62. Onofri S, Selbmann L, Pacelli C, Zucconi L, Rabbow E, de Vera J-P (2018b) Survival, DNA, and ultrastructural integrity of a cryptoendolithic Antarctic fungus in Mars and lunar rock analogues exposed outside the International Space Station. Astrobiology.  https://doi.org/10.1089/ast.2017.1728
  63. Pierson DL (2001) Microbial contamination of spacecraft. Gravit Space Biol Bull 14:1–6Google Scholar
  64. Plubell DL, Wilmarth PA, Zhao Y, Fenton AM, Minnier J, Reddy AP, Klimek J, Yang X, David LL, Pamir N (2017) Extended multiplexing of tandem mass tags (TMT) labeling reveals age and high fat diet specific proteome changes in mouse epididymal adipose tissue. Mol Cell Proteomics 16:873–890.  https://doi.org/10.1074/mcp.M116.065524 CrossRefGoogle Scholar
  65. Pusztahelyi T, Klement É, Szajli E, Klem J, Miskei M, Karányi Z, Emri T, Kovács S, Orosz G, Kovács KL, Medzihradszky KF, Prade RA, Pócsi I (2011) Comparison of transcriptional and translational changes caused by long-term menadione exposure in Aspergillus nidulans. Fungal Genet Biol 48:92–103.  https://doi.org/10.1016/j.fgb.2010.08.006 CrossRefGoogle Scholar
  66. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11:R25.  https://doi.org/10.1186/gb-2010-11-3-r25 CrossRefGoogle Scholar
  67. Sanchez JF, Entwistle R, Hung J-H, Yaegashi J, Jain S, Chiang Y-M, Wang CCC, Oakley BR (2011) Genome-based deletion analysis reveals the prenyl xanthone biosynthesis pathway in Aspergillus nidulans. J Am Chem Soc 133:4010–4017.  https://doi.org/10.1021/ja1096682 CrossRefGoogle Scholar
  68. Sanchez JF, Somoza AD, Keller NP, Wang CCC (2012) Advances in Aspergillus secondary metabolite research in the post-genomic era. Nat Prod Rep 29:351–371.  https://doi.org/10.1039/c2np00084a CrossRefGoogle Scholar
  69. Segal BH (2009) Aspergillosis. N Engl J Med 360:1870–1884.  https://doi.org/10.1056/NEJMra0808853 CrossRefGoogle Scholar
  70. Sharpe RA, Bearman N, Thornton CR, Husk K, Osborne NJ (2015) Indoor fungal diversity and asthma: a meta-analysis and systematic review of risk factors. J Allergy Clin Immunol 135:110–122.  https://doi.org/10.1016/j.jaci.2014.07.002 CrossRefGoogle Scholar
  71. Singaravelan N, Grishkan I, Beharav A, Wakamatsu K, Ito S, Nevo E (2008) Adaptive melanin response of the soil fungus Aspergillus niger to UV radiation stress at “Evolution Canyon”, Mount Carmel, Israel. PLoS One 3:e2993.  https://doi.org/10.1371/journal.pone.0002993 CrossRefGoogle Scholar
  72. Stajich JE, Harris T, Brunk BP, Brestelli J, Fischer S, Harb OS, Kissinger JC, Li W, Nayak V, Pinney DF, Stoeckert CJ, Roos DS (2012) FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Res 40:D675–D681.  https://doi.org/10.1093/nar/gkr918 CrossRefGoogle Scholar
  73. Szewczyk E, Nayak T, Oakley CE, Edgerton H, Xiong Y, Taheri-Talesh N, Osmani SA, Oakley BR, Oakley B (2006) Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 1:3111–3120.  https://doi.org/10.1038/nprot.2006.405 CrossRefGoogle Scholar
  74. Szewczyk E, Chiang Y-M, Oakley CE, Davidson AD, Wang CCC, Oakley BR (2008) Identification and characterization of the asperthecin gene cluster of Aspergillus nidulans. Appl Environ Microbiol 74:7607–7612.  https://doi.org/10.1128/AEM.01743-08 CrossRefGoogle Scholar
  75. Tixador R, Richoilley G, Gasset G, Templier J, Bes J, Moatti N, Lapchine L (1985) Study of minimal inhibitory concentration of antibiotics on bacteria cultivated in vitro in space (Cytos 2 experiment). Aviat Space Environ Med 56:748–751Google Scholar
  76. Tkavc R, Matrosova VY, Grichenko OE, Gostinčar C, Volpe RP, Klimenkova P, Gaidamakova EK, Zhou CE, Stewart BJ, Lyman MG, Malfatti SA, Rubinfeld B, Courtot M, Singh J, Dalgard CL, Hamilton T, Frey KG, Gunde-Cimerman N, Dugan L, Daly MJ (2018) Prospects for fungal bioremediation of acidic radioactive waste sites: characterization and genome sequence of Rhodotorula taiwanensis MD1149. Front Microbiol 8.  https://doi.org/10.3389/fmicb.2017.02528
  77. Uhl MA, Biery M, Craig N, Johnson AD (2003) Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C. albicans. EMBO J 22:2668–2678.  https://doi.org/10.1093/emboj/cdg256 CrossRefGoogle Scholar
  78. Van Houdt R, Mijnendonckx K, Leys N (2012) Microbial contamination monitoring and control during human space missions. Planet Space Sci 60:115–120.  https://doi.org/10.1016/j.pss.2011.09.001 CrossRefGoogle Scholar
  79. Venkateswaran K, Vaishampayan P, Cisneros J, Pierson DL, Rogers SO, Perry J (2014) International Space Station environmental microbiome—microbial inventories of ISS filter debris. Appl Microbiol Biotechnol 98:6453–6466.  https://doi.org/10.1007/s00253-014-5650-6 CrossRefGoogle Scholar
  80. Volz PA, Dublin M (1973) Filamentous fungi exposed to spaceflight stresses including known levels of ultraviolet irradiations. Space Life Sci 4:402–414.  https://doi.org/10.1007/BF00930352 Google Scholar
  81. de Vries RP, Visser J (2001) Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev 65:497–522.  https://doi.org/10.1128/MMBR.65.4.497-522.2001 CrossRefGoogle Scholar
  82. Wilson JW, Ott CM, Quick L, Davis R, zu Bentrup KH, Crabbé A, Richter E, Sarker S, Barrila J, Porwollik S, Cheng P, McClelland M, Tsaprailis G, Radabaugh T, Hunt A, Shah M, Nelman-Gonzalez M, Hing S, Parra M, Dumars P, Norwood K, Bober R, Devich J, Ruggles A, CdeBaca A, Narayan S, Benjamin J, Goulart C, Rupert M, Catella L, Schurr MJ, Buchanan K, Morici L, McCracken J, Porter MD, Pierson DL, Smith SM, Mergeay M, Leys N, Stefanyshyn-Piper HM, Gorie D, Nickerson CA (2008) Media ion composition controls regulatory and virulence response of Salmonella in spaceflight. PLoS One 3:e3923.  https://doi.org/10.1371/journal.pone.0003923 CrossRefGoogle Scholar
  83. Wu J, Wang M, Zhou L, Yu D (2016) Small heat shock proteins, phylogeny in filamentous fungi and expression analyses in Aspergillus nidulans. Gene 575:675–679.  https://doi.org/10.1016/j.gene.2015.09.044 CrossRefGoogle Scholar
  84. Yaegashi J, Oakley BR, Wang CCC (2014) Recent advances in genome mining of secondary metabolite biosynthetic gene clusters and the development of heterologous expression systems in Aspergillus nidulans. J Ind Microbiol Biotechnol 41:433–442.  https://doi.org/10.1007/s10295-013-1386-z CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Jillian Romsdahl
    • 1
  • Adriana Blachowicz
    • 1
    • 2
  • Abby J. Chiang
    • 3
  • Yi-Ming Chiang
    • 1
  • Sawyer Masonjones
    • 4
  • Junko Yaegashi
    • 1
  • Stefanie Countryman
    • 5
  • Fathi Karouia
    • 6
    • 7
  • Markus Kalkum
    • 3
  • Jason E. Stajich
    • 4
  • Kasthuri Venkateswaran
    • 2
  • Clay C. C. Wang
    • 1
    • 8
    Email author
  1. 1.Department of Pharmacology and Pharmaceutical Sciences, School of PharmacyUniversity of Southern CaliforniaLos AngelesUSA
  2. 2.Biotechnology and Planetary Protection Group, Jet Propulsion LaboratoryCalifornia Institute of TechnologyPasadenaUSA
  3. 3.Department of Molecular Imaging and TherapyBeckman Research Institute of City of HopeDuarteUSA
  4. 4.Department of Microbiology & Plant Pathology and Institute of Integrative Genome BiologyUniversity of California-RiversideRiversideUSA
  5. 5.BioServe Space TechnologiesUniversity of ColoradoBoulderUSA
  6. 6.Space Biosciences DivisionNASA Ames Research CenterMountain ViewUSA
  7. 7.Department of Pharmaceutical Chemistry, School of PharmacyUniversity of California San FranciscoSan FranciscoUSA
  8. 8.Department of Chemistry, College of Letters, Arts, and SciencesUniversity of Southern CaliforniaLos AngelesUSA

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