Applied Microbiology and Biotechnology

, Volume 99, Issue 8, pp 3715–3728 | Cite as

Biosynthesis and genomic analysis of medium-chain hydrocarbon production by the endophytic fungal isolate Nigrograna mackinnonii E5202H

  • Jeffery J. Shaw
  • Daniel J. Spakowicz
  • Rahul S. Dalal
  • Jared H. Davis
  • Nina A. Lehr
  • Brian F. Dunican
  • Esteban A. Orellana
  • Alexandra Narváez-Trujillo
  • Scott A. Strobel
Bioenergy and biofuels


An endophytic fungus was isolated that produces a series of volatile natural products, including terpenes and odd chain polyenes. Phylogenetic analysis of the isolate using five loci suggests that it is closely related to Nigrograna mackinnonii CBS 674.75. The main component of the polyene series was purified and identified as (3E,5E,7E)-nona-1,3,5,7-tetraene (NTE), a novel natural product. Non-oxygenated hydrocarbons of this chain length are uncommon and desirable as gasoline-surrogate biofuels. The biosynthetic pathway for NTE production was explored using metabolic labeling and gas chromatography time of flight mass spectometer (GCMS). Two-carbon incorporation 13C acetate suggests that it is derived from a polyketide synthase (PKS) followed by decarboxylation. There are several known mechanisms for such decarboxylation, though none have been discovered in fungi. Towards identifying the PKS responsible for the production of NTE, the genome of N. mackinnonii E5202H (ATCC SD-6839) was sequenced and assembled. Of the 32 PKSs present in the genome, 17 are predicted to contain sufficient domains for the production of NTE. These results exemplify the capacity of endophytic fungi to produce novel natural products that may have many uses, such as biologically derived fuels and commodity chemicals.


Endophyte Natural product Volatile organic compound Polyene Medium-chain hydrocarbon Biofuel Polyketide synthase 



This research was performed with a collecting and research permit provided to SAS by the Ministerio del Ambiente of Ecuador. The authors would like to thank Percy Vargas Nunez for help with collection and identification of the host plant, Gary Strobel for the M. albus isolate used for the selection, Joseph Wolenski for providing the microscope facilities, Nicholas J. Carriero, and Robert D. Bjornson in the Yale University Biomedical High Performance Computing Center funded by NIH grants RR19895 and RR029676-01, and the Office of Assistant Secretary of Defense for Research and Engineering NSSEFF grant N00244-09-1-0070 awarded to SAS. DJS and BFD were supported in part by the NIH Cell and Molecular Biology training grant number T32 GM007223.

Supplementary material

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  1. Ahlert J, Shepard E, Lomovskaya N, Zazopoulos E, Staffa A, Bachmann BO, Huang K, Fonstein L, Czisny A, Whitwam RE, Farnet CM, Thorson JS (2002) The calicheamicin gene cluster and its iterative type I enediyne PKS. Science 297:1173–1176. doi: 10.1126/science.1072105 CrossRefPubMedGoogle Scholar
  2. Alonso-Gutierrez J, Chan R, Batth TS, Adams PD, Keasling JD, Petzold CJ, Lee TS (2013) Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production. Metab Eng 19C:33–41. doi: 10.1016/j.ymben.2013.05.004 CrossRefGoogle Scholar
  3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedCentralPubMedGoogle Scholar
  4. Aly AH, Debbab A, Proksch P (2011) Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90:1829–1845. doi: 10.1007/s00253-011-3270-y CrossRefPubMedGoogle Scholar
  5. Aparicio JF, Mendes MV, Antón N, Recio E, Martín JF (2004) Polyene macrolide antibiotic biosynthesis. Curr Med Chem 11:1645–1656CrossRefPubMedGoogle Scholar
  6. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549CrossRefPubMedGoogle Scholar
  7. Arnold A e, Maynard Z, Gilbert G s, Coley P d, Kursar T a (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274. doi: 10.1046/j.1461-0248.2000.00159.x CrossRefGoogle Scholar
  8. Atsumi S, Hanai T, Liao JC (2008) Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451:86–89. doi: 10.1038/nature06450 CrossRefPubMedGoogle Scholar
  9. Beller HR, Goh E-B, Keasling JD (2010) Genes involved in long-chain alkene biosynthesis in Micrococcus luteus. Appl Environ Microbiol 76:1212–1223. doi: 10.1128/AEM. 02312-09 CrossRefPubMedCentralPubMedGoogle Scholar
  10. Block E, Aslam M, Eswarakrishnan V, Gebreyes K, Hutchinson J, Iyer R, Laffitte JA, Wall A (1986) Alpha.-Haloalkanesulfonyl bromides in organic synthesis. 5. Versatile reagents for the synthesis of conjugated polyenes, enones, and 1,3-oxathiole 1,1-dioxides. J Am Chem Soc 108:4568–4580. doi: 10.1021/ja00275a051 CrossRefGoogle Scholar
  11. Bolard J (1986) How do the polyene macrolide antibiotics affect the cellular membrane properties? Biochim Biophys Acta 864:257–304CrossRefPubMedGoogle Scholar
  12. Borelli D (1976) Pyrenochaeta mackinnonii nova species agente de micetoma. Castellania 4:227–234Google Scholar
  13. Castoe TA, Stephens T, Noonan BP, Calestani C (2007) A novel group of type I polyketide synthases (PKS) in animals and the complex phylogenomics of PKSs. Gene 392:47–58. doi: 10.1016/j.gene.2006.11.005 CrossRefPubMedGoogle Scholar
  14. Chitarra GS, Abee T, Rombouts FM, Posthumus MA, Dijksterhuis J (2004) Germination of Penicillium paneum Conidia is regulated by 1-Octen-3-ol, a volatile self-inhibitor. Appl Environ Microbiol 70:2823–2829. doi: 10.1128/AEM. 70.5.2823-2829.2004 CrossRefPubMedCentralPubMedGoogle Scholar
  15. Combet E, Henderson J, Eastwood DC, Burton KS (2006) Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47:317–326. doi: 10.1007/s10267-006-0318-4 CrossRefGoogle Scholar
  16. Connor MR, Liao JC (2009) Microbial production of advanced transportation fuels in non-natural hosts. Curr Opin Biotechnol 20:307–315. doi: 10.1016/j.copbio.2009.04.002 CrossRefPubMedGoogle Scholar
  17. Connor MR, Cann AF, Liao JC (2010) 3-Methyl-1-butanol production in Escherichia coli: random mutagenesis and two-phase fermentation. Appl Microbiol Biotechnol 86:1155–1164. doi: 10.1007/s00253-009-2401-1 CrossRefPubMedCentralPubMedGoogle Scholar
  18. De Gruyter J, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, Crous PW (2013) Redisposition of phoma-like anamorphs in Pleosporales. Stud Mycol 75:1–36. doi: 10.3114/sim0004 CrossRefPubMedCentralPubMedGoogle Scholar
  19. Ezra D, Hess WM, Strobel GA (2004) New endophytic isolates of Muscodor albus, a volatile-antibiotic-producing fungus. Microbiology 150:4023–4031. doi: 10.1099/mic. 0.27334-0 CrossRefPubMedGoogle Scholar
  20. Felnagle EA, Chaubey A, Noey EL, Houk KN, Liao JC (2012) Engineering synthetic recursive pathways to generate non-natural small molecules. Nat Chem Biol 8:518–526. doi: 10.1038/nchembio.959 CrossRefPubMedGoogle Scholar
  21. Fernandes C, Catrinescu C, Castilho P, Russo PA, Carrott MR, Breen C (2007) Catalytic conversion of limonene over acid activated Serra de Dentro (SD) bentonite. Appl Catal Gen 318:108–120. doi: 10.1016/j.apcata.2006.10.048 CrossRefGoogle Scholar
  22. Fiedler K, Schütz E, Geh S (2001) Detection of microbial volatile organic compounds (MVOCs) produced by moulds on various materials. Int J Hyg Environ Health 204:111–121. doi: 10.1078/1438-4639-00094 CrossRefPubMedGoogle Scholar
  23. Fortman JL, Chhabra S, Mukhopadhyay A, Chou H, Lee TS, Steen E, Keasling JD (2008) Biofuel alternatives to ethanol: pumping the microbial well. Trends Biotechnol 26:375–381. doi: 10.1016/j.tibtech.2008.03.008 CrossRefPubMedGoogle Scholar
  24. Frankel EN, Neff WE, Selke E (1981) Analysis of autoxidized fats by gas chromatography-mass spectrometry: VII. Volatile thermal decomposition products of pure hydroperoxides from autoxidized and photosensitized oxidized methyl oleate, linoleate and linolenate. Lipids 16:279–285. doi: 10.1007/BF02534950 CrossRefGoogle Scholar
  25. Gabler FM, Mercier J, Jiménez JI, Smilanick JL (2010) Integration of continuous biofumigation with Muscodor albus with pre-cooling fumigation with ozone or sulfur dioxide to control postharvest gray mold of table grapes. Postharvest Biol Technol 55:78–84. doi: 10.1016/j.postharvbio.2009.07.012 CrossRefGoogle Scholar
  26. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414. doi: 10.1038/nchembio.2007.5 CrossRefPubMedGoogle Scholar
  27. Geu-Flores F, Sherden NH, Courdavault V, Burlat V, Glenn WS, Wu C, Nims E, Cui Y, O’Connor SE (2012) An alternative route to cyclic terpenes by reductive cyclization in iridoid biosynthesis. Nature 492:138–142. doi: 10.1038/nature11692 CrossRefPubMedGoogle Scholar
  28. Gianoulis TA, Griffin MA, Spakowicz DJ, Dunican BF, Alpha CJ, Sboner A, Sismour AM, Kodira C, Egholm M, Church GM, Gerstein MB, Strobel SA (2012) Genomic analysis of the hydrocarbon-producing, cellulolytic, endophytic fungus Ascocoryne sarcoides. PLoS Genet 8:e1002558. doi: 10.1371/journal.pgen.1002558 CrossRefPubMedCentralPubMedGoogle Scholar
  29. Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, Berlin AM, Aird D, Costello M, Daza R, Williams L, Nicol R, Gnirke A, Nusbaum C, Lander ES, Jaffe DB (2010) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci 201017351. doi: 10.1073/pnas.1017351108
  30. Griffin MA, Spakowicz DJ, Gianoulis TA, Strobel SA (2010) Volatile organic compound production by organisms in the genus Ascocoryne and a re-evaluation of myco-diesel production by NRRL 50072. Microbiology 156:3814–3829. doi: 10.1099/mic. 0.041327-0 CrossRefPubMedGoogle Scholar
  31. Gu L, Wang B, Kulkarni A, Gehret JJ, Lloyd KR, Gerwick L, Gerwick WH, Wipf P, Håkansson K, Smith JL, Sherman DH (2009) Polyketide decarboxylative chain termination preceded by o-sulfonation in curacin a biosynthesis. J Am Chem Soc 131:16033–16035. doi: 10.1021/ja9071578 CrossRefPubMedCentralPubMedGoogle Scholar
  32. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56. doi: 10.1038/nrmicro797 CrossRefPubMedGoogle Scholar
  33. Harvey BG, Wright ME, Quintana RL (2010) High-density renewable fuels based on the selective dimerization of Pinenes. Energy Fuel 24:267–273. doi: 10.1021/ef900799c CrossRefGoogle Scholar
  34. Horsman GP, Van Lanen SG, Shen B (2009) Chapter 5 iterative type I polyketide synthases for enediyne core biosynthesis. In: Hopwood DA (ed) Methods Enzymol. Academic Press, pp 97–112Google Scholar
  35. Hyde KD, Borse BD (1986) Marine fungi from Seychelles: 5 Biatriospora marina gen. and sp. nov. from mangrove woodGoogle Scholar
  36. Keitel J, Fischer-Lui I, Boland W, Müller DG (1990) Novel C9 and C11 hydrocarbons from the Brown Alga Cutleria multifida; sigmatropic and electrocyclic reactions in nature. Part VI. Helv Chim Acta 73:2101–2112. doi: 10.1002/hlca.19900730806 CrossRefGoogle Scholar
  37. Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, Fedorova ND (2010) SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol FGB 47:736–741. doi: 10.1016/j.fgb.2010.06.003 CrossRefGoogle Scholar
  38. Kirk PM, Ainsworth GC (2008) Ainsworth & Bisby’s dictionary of the fungi. CABIGoogle Scholar
  39. Korpi A, Järnberg J, Pasanen A-L (2009) Microbial volatile organic compounds. Crit Rev Toxicol 39:139–193. doi: 10.1080/10408440802291497 CrossRefPubMedGoogle Scholar
  40. Kroumova AB, Xie Z, Wagner GJ (1994) A pathway for the biosynthesis of straight and branched, odd- and even-length, medium-chain fatty acids in plants. Proc Natl Acad Sci 91:11437–11441CrossRefPubMedCentralPubMedGoogle Scholar
  41. Lancker FV, Adams A, Delmulle B, Saeger SD, Moretti A, Peteghem CV, Kimpe ND (2008) Use of headspace SPME-GC-MS for the analysis of the volatiles produced by indoor molds grown on different substrates. J Environ Monit 10:1127–1133. doi: 10.1039/B808608G CrossRefPubMedGoogle Scholar
  42. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. doi: 10.1038/nmeth.1923 CrossRefPubMedCentralPubMedGoogle Scholar
  43. Larsen TO, Frisvad JC (1995) Characterization of volatile metabolites from 47 Penicillium taxa. Mycol Res 99:1153–1166. doi: 10.1016/S0953-7562(09)80271-2 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 Oxford Engl 25:2078–2079. doi: 10.1093/bioinformatics/btp352 CrossRefGoogle Scholar
  45. Liu W, Christenson SD, Standage S, Shen B (2002) Biosynthesis of the enediyne antitumor antibiotic C-1027. Science 297:1170–1173. doi: 10.1126/science.1072110 CrossRefPubMedGoogle Scholar
  46. Liu W, Nonaka K, Nie L, Zhang J, Christenson SD, Bae J, Van Lanen SG, Zazopoulos E, Farnet CM, Yang CF, Shen B (2005) The neocarzinostatin biosynthetic gene cluster from Streptomyces carzinostaticus ATCC 15944 involving two iterative type I polyketide synthases. Chem Biol 12:293–302. doi: 10.1016/j.chembiol.2004.12.013 CrossRefPubMedGoogle Scholar
  47. McElvain SM, Bright RD, Johnson PR (1941) The constituents of the volatile oil of catnip. I. Nepetalic acid, nepetalactone and related compounds. J Am Chem Soc 63:1558–1563. doi: 10.1021/ja01851a019 CrossRefGoogle Scholar
  48. Mendez-Perez D, Begemann MB, Pfleger BF (2011) Modular synthase-encoding gene involved in α-olefin biosynthesis in Synechococcus sp. strain PCC 7002. Appl Environ Microbiol 77:4264–4267. doi: 10.1128/AEM. 00467-11 CrossRefPubMedCentralPubMedGoogle Scholar
  49. Mitchell AM, Strobel GA, Moore E, Robison R, Sears J (2010) Volatile antimicrobials from Muscodor crispans, a novel endophytic fungus. Microbiol Read Engl 156:270–277. doi: 10.1099/mic. 0.032540-0 CrossRefGoogle Scholar
  50. Müller DG, Jaenicke L, Donike M, Akintobi T (1971) Sex attractant in a brown alga: chemical structure. Science 171:815–817. doi: 10.1126/science.171.3973.815 CrossRefPubMedGoogle Scholar
  51. Peralta-Yahya PP, Keasling JD (2010) Advanced biofuel production in microbes. Biotechnol J 5:147–162. doi: 10.1002/biot.200900220 CrossRefPubMedGoogle Scholar
  52. Peralta-Yahya PP, Ouellet M, Chan R, Mukhopadhyay A, Keasling JD, Lee TS (2011) Identification and microbial production of a terpene-based advanced biofuel. Nat Commun 2:483. doi: 10.1038/ncomms1494 CrossRefPubMedCentralPubMedGoogle Scholar
  53. Peralta-Yahya PP, Zhang F, del Cardayre SB, Keasling JD (2012) Microbial engineering for the production of advanced biofuels. Nature 488:320–328. doi: 10.1038/nature11478 CrossRefPubMedGoogle Scholar
  54. Pohnert G, Boland W (1994) Pericyclic reactions in nature: evidence for a spontaneous [1.7]-hydrogen shift and an 8πe electrocyclic ring closure in the biosynthesis of olefinic hydrocarbons from marine brown algae (Phaeophyceae). Tetrahedron 50:10235–10244. doi: 10.1016/S0040-4020(01)81756-7 CrossRefGoogle Scholar
  55. Polizzi V, Adams A, Malysheva SV, De Saeger S, Van Peteghem C, Moretti A, Picco AM, De Kimpe N (2012) Identification of volatile markers for indoor fungal growth and chemotaxonomic classification of Aspergillus species. Fungal Biol 116:941–953. doi: 10.1016/j.funbio.2012.06.001 CrossRefPubMedGoogle Scholar
  56. Pourbafrani M, Forgács G, Horváth IS, Niklasson C, Taherzadeh MJ (2010) Production of biofuels, limonene and pectin from citrus wastes. Bioresour Technol 101:4246–4250. doi: 10.1016/j.biortech.2010.01.077 CrossRefPubMedGoogle Scholar
  57. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD (2012) The PFAM protein families database. Nucleic Acids Res 40:D290–D301. doi: 10.1093/nar/gkr1065 CrossRefPubMedCentralPubMedGoogle Scholar
  58. Qiu Y, Tittiger C, Wicker-Thomas C, Goff GL, Young S, Wajnberg E, Fricaux T, Taquet N, Blomquist GJ, Feyereisen R (2012) An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc Natl Acad Sci 109:14858–14863. doi: 10.1073/pnas.1208650109 CrossRefPubMedCentralPubMedGoogle Scholar
  59. Redding-Johanson AM, Batth TS, Chan R, Krupa R, Szmidt HL, Adams PD, Keasling JD, Soon Lee T, Mukhopadhyay A, Petzold CJ (2011) Targeted proteomics for metabolic pathway optimization: application to terpene production. Metab Eng 13:194–203. doi: 10.1016/j.ymben.2010.12.005 CrossRefPubMedGoogle Scholar
  60. Riyaz-Ul-Hassan S, Strobel G, Geary B, Sears J (2013) An endophytic Nodulisporium sp. from Central America producing volatile organic compounds with both biological and fuel potential. J Microbiol Biotechnol 23:29–35CrossRefPubMedGoogle Scholar
  61. Rude MA, Baron TS, Brubaker S, Alibhai M, Del Cardayre SB, Schirmer A (2011) Terminal olefin (1-alkene) biosynthesis by a novel p450 fatty acid decarboxylase from Jeotgalicoccus species. Appl Environ Microbiol 77:1718–1727. doi: 10.1128/AEM. 02580-10 CrossRefPubMedCentralPubMedGoogle Scholar
  62. Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB (2010) Microbial biosynthesis of alkanes. Science 329:559–562. doi: 10.1126/science.1187936 CrossRefPubMedGoogle Scholar
  63. Schoch CL, Crous PW, Groenewald JZ, Boehm EWA, Burgess TI, De Gruyter J, De Hoog GS, Dixon LJ, Grube M, Gueidan C, Harada Y, Hatakeyama S, Hirayama K, Hosoya T, Huhndorf SM, Hyde KD, Jones EBG, Kohlmeyer J, Kruys A, Li YM, Lücking R, Lumbsch HT, Marvanová L, Mbatchou JS, McVay AH, Miller AN, Mugambi GK, Muggia L, Nelsen MP, Nelson P, Owensby CA, Phillips AJL, Phongpaichit S, Pointing SB, Pujade-Renaud V, Raja HA, Plata ER, Robbertse B, Ruibal C, Sakayaroj J, Sano T, Selbmann L, Shearer CA, Shirouzu T, Slippers B, Suetrong S, Tanaka K, Volkmann-Kohlmeyer B, Wingfield MJ, Wood AR, Woudenberg JHC, Yonezawa H, Zhang Y, Spatafora JW (2009) A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64, 1–15–S10. doi: 10.3114/sim.2009.64.01 CrossRefPubMedCentralGoogle Scholar
  64. Schuchardt S, Kruse H (2009) Quantitative volatile metabolite profiling of common indoor fungi: relevancy for indoor air analysis. J Basic Microbiol 49:350–362. doi: 10.1002/jobm.200800152 CrossRefPubMedGoogle Scholar
  65. Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7:285–295CrossRefPubMedGoogle Scholar
  66. Spangler CW, Little DA (1982) Synthesis and characterization of representative octa-1,3,5,7-tetraenes and deca-1,3,5,7,9-pentaenes. J Chem Soc [Perkin] 1:2379–2385. doi: 10.1039/P19820002379 CrossRefGoogle Scholar
  67. Spangler CW, McCoy RK, Karavakis AA (1986) 3-Alkoxypropenals as precursors in the synthesis of conjugated and semiconjugated polyenes: methyl-substituted octa- and nona-tetraenes. J Chem Soc [Perkin] 1:1203–1207. doi: 10.1039/P19860001203 CrossRefGoogle Scholar
  68. Stoppacher N, Kluger B, Zeilinger S, Krska R, Schuhmacher R (2010) Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J Microbiol Methods 81:187–193. doi: 10.1016/j.mimet.2010.03.011 CrossRefPubMedGoogle Scholar
  69. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502. doi: 10.1128/MMBR. 67.4.491-502.2003 CrossRefPubMedCentralPubMedGoogle Scholar
  70. Strobel GA, Dirkse E, Sears J, Markworth C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiol Read Engl 147:2943–2950Google Scholar
  71. Strobel GA, Knighton B, Kluck K, Ren Y, Livinghouse T, Griffin M, Spakowicz D, Sears J (2008) The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 154:3319–3328. doi: 10.1099/mic. 0.2008/022186-0 CrossRefPubMedGoogle Scholar
  72. Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M (2008) Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res 18:1979–1990. doi: 10.1101/gr.081612.108 CrossRefPubMedCentralPubMedGoogle Scholar
  73. Tess Mends M, Yu E (2012) An endophytic Nodulisporium sp. producing volatile organic compounds having bioactivity and fuel potential. J Pet Environ Biotechnol. doi: 10.4172/2157-7463.1000117 Google Scholar
  74. Tomsheck AR, Strobel GA, Booth E, Geary B, Spakowicz D, Knighton B, Floerchinger C, Sears J, Liarzi O, Ezra D (2010) Hypoxylon sp., an endophyte of Persea indica, producing 1,8-cineole and other bioactive volatiles with fuel potential. Microb Ecol 60:903–914. doi: 10.1007/s00248-010-9759-6 CrossRefPubMedGoogle Scholar
  75. Tressl R, Bahri D, Engel KH (1982) Formation of eight-carbon and ten-carbon components in mushrooms (Agaricus campestris). J Agric Food Chem 30:89–93CrossRefGoogle Scholar
  76. Ul-Hassan SR, Strobel GA, Booth E, Knighton B, Floerchinger C, Sears J (2012) Modulation of volatile organic compound formation in the Mycodiesel-producing endophyte Hypoxylon sp. CI-4. Microbiol Read Engl 158:465–473. doi: 10.1099/mic. 0.054643-0 CrossRefGoogle Scholar
  77. Van Lanen SG, Oh T, Liu W, Wendt-Pienkowski E, Shen B (2007) Characterization of the maduropeptin biosynthetic gene cluster from Actinomadura madurae ATCC 39144 supporting a unifying paradigm for enediyne biosynthesis. J Am Chem Soc 129:13082–13094. doi: 10.1021/ja073275o CrossRefPubMedCentralPubMedGoogle Scholar
  78. Wheatley R, Hackett C, Bruce A, Kundzewicz A (1997) Effect of substrate composition on production of volatile organic compounds from Trichoderma spp. Inhibitory to wood decay fungi. Int Biodeterior Biodegrad 39:199–205. doi: 10.1016/S0964-8305(97)00015-2 CrossRefGoogle Scholar
  79. Wihlborg R, Pippitt D, Marsili R (2008) Headspace sorptive extraction and GC-TOFMS for the identification of volatile fungal metabolites. J Microbiol Methods 75:244–250. doi: 10.1016/j.mimet.2008.06.011 CrossRefPubMedGoogle Scholar
  80. Wurzenberger M, Grosch W (1984) The formation of 1-octen-3-ol from the 10-hydroperoxide isomer of linoleic acid by a hydroperoxide lyase in mushrooms (Psalliota bispora). Biochim Biophys Acta BBA Lipids Lipid Metab 794:25–30CrossRefGoogle Scholar
  81. Zhang J, Lanen SGV, Ju J, Liu W, Dorrestein PC, Li W, Kelleher NL, Shen B (2008) A phosphopantetheinylating polyketide synthase producing a linear polyene to initiate enediyne antitumor antibiotic biosynthesis. Proc Natl Acad Sci 105:1460–1465. doi: 10.1073/pnas.0711625105 CrossRefPubMedCentralPubMedGoogle Scholar
  82. Zhang Y, Schoch CL, Fournier J, Crous PW, De Gruyter J, Woudenberg JH, Hirayama K, Tanaka K, Pointing SB, Spatafora JW, Hyde KD (2009) Multi-locus phylogeny of Pleosporales: a taxonomic, ecological and evolutionary re-evaluation. Stud Mycol 64, 85–102–S5. doi: 10.3114/sim.2009.64.04 CrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jeffery J. Shaw
    • 1
  • Daniel J. Spakowicz
    • 1
  • Rahul S. Dalal
    • 1
  • Jared H. Davis
    • 1
  • Nina A. Lehr
    • 1
  • Brian F. Dunican
    • 1
  • Esteban A. Orellana
    • 2
  • Alexandra Narváez-Trujillo
    • 2
  • Scott A. Strobel
    • 1
  1. 1.Department of Molecular Biophysics and BiochemistryYale UniversityNew HavenUSA
  2. 2.Laboratorio de Biotecnología VegetalPontificia Universidad Católica del EcuadorQuitoEcuador

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