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

  • Bioenergy and biofuels
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Abstract

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.

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References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 25:3389–3402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Aparicio JF, Mendes MV, Antón N, Recio E, Martín JF (2004) Polyene macrolide antibiotic biosynthesis. Curr Med Chem 11:1645–1656

    Article  CAS  PubMed  Google Scholar 

  • Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bolard J (1986) How do the polyene macrolide antibiotics affect the cellular membrane properties? Biochim Biophys Acta 864:257–304

    Article  CAS  PubMed  Google Scholar 

  • Borelli D (1976) Pyrenochaeta mackinnonii nova species agente de micetoma. Castellania 4:227–234

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 97–112

  • Hyde KD, Borse BD (1986) Marine fungi from Seychelles: 5 Biatriospora marina gen. and sp. nov. from mangrove wood

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kirk PM, Ainsworth GC (2008) Ainsworth & Bisby’s dictionary of the fungi. CABI

  • Korpi A, Järnberg J, Pasanen A-L (2009) Microbial volatile organic compounds. Crit Rev Toxicol 39:139–193. doi:10.1080/10408440802291497

    Article  CAS  PubMed  Google Scholar 

  • 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 91:11437–11441

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. doi:10.1038/nmeth.1923

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Peralta-Yahya PP, Keasling JD (2010) Advanced biofuel production in microbes. Biotechnol J 5:147–162. doi:10.1002/biot.200900220

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 23:29–35

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7:285–295

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Strobel GA, Dirkse E, Sears J, Markworth C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiol Read Engl 147:2943–2950

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tressl R, Bahri D, Engel KH (1982) Formation of eight-carbon and ten-carbon components in mushrooms (Agaricus campestris). J Agric Food Chem 30:89–93

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 794:25–30

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, 06511, USA

    Jeffery J. Shaw, Daniel J. Spakowicz, Rahul S. Dalal, Jared H. Davis, Nina A. Lehr, Brian F. Dunican & Scott A. Strobel

  2. Laboratorio de Biotecnología Vegetal, Pontificia Universidad Católica del Ecuador, Quito, Ecuador

    Esteban A. Orellana & Alexandra Narváez-Trujillo

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  1. Jeffery J. Shaw
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Correspondence to Scott A. Strobel.

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Jeffery J. Shaw and Daniel J. Spakowicz contributed equally to this work.

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Shaw, J.J., Spakowicz, D.J., Dalal, R.S. et al. Biosynthesis and genomic analysis of medium-chain hydrocarbon production by the endophytic fungal isolate Nigrograna mackinnonii E5202H. Appl Microbiol Biotechnol 99, 3715–3728 (2015). https://doi.org/10.1007/s00253-014-6206-5

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