Genomic analysis of the hydrocarbon-producing, cellulolytic, endophytic fungus ascocoryne sarcoides

PLoS Genetics

Volumn 8, Issue 3, 2012, Pages

  Gianoulis, Tara A ^a,b,c   Griffin, Meghan A ^c   Spakowicz, Daniel J ^c   Dunican, Brian F ^c   Alpha, Cambria J ^c   Sboner, Andrea ^c   Michael Sismour, A ^a,b   Kodira, Chinnappa ^d   Egholm, Michael ^e   Church, George M ^a,b   Gerstein, Mark B ^c   Strobel, Scott A ^c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c YALE UNIVERSITY   (United States)

^d Roche 454 Life Sciences   (United States)

^e PALL CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFUEL; CELLULOSE; UNTRANSLATED RNA; HYDROCARBON; TRANSCRIPTOME;

ARTICLE; ASCOCORYNE SARCOIDES; BIOFUEL PRODUCTION; CONTROLLED STUDY; ENDOPHYTE; FUNGAL GENE; FUNGAL METABOLISM; FUNGAL STRAIN; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENETIC ANALYSIS; METABOLOMICS; NONHUMAN; TRANSCRIPTOMICS; ASCOMYCETES; FUNGAL GENOME; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; REVERSE GENETICS; SEQUENCE ANALYSIS;

ASCOCORYNE SARCOIDES; FUNGI;

ASCOMYCOTA; BIOFUELS; CELLULOSE; ENDOPHYTES; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; HYDROCARBONS; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; REVERSE GENETICS; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84859239291     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002558     Document Type: Article

References (77)

1. Sarpal AS, Kapur GS, Mukherjee S, Tiwari AK, (2001) PONA analyses of cracked gasoline by 1H NMR spectroscopy. Part II. Fuel 80: 521-528 doi:10.1016/S0016-2361(00)00123-X.
2. Murahashi S, (1938) \Über die riechstoffe des matsutake (Armillaria Matsutake Ito et Imai Agaricaceae). Sci Pap Inst Phys Chem Res(Tokyo) 34: 155-172.
3. 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.
4. Strobel GA, Knighton B, Kluck K, Ren Y, Livinghouse T, et al. (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.
5. Griffin MA, Spakowicz DJ, Gianoulis TA, Strobel SA, (2010) Volatile organic compound production by organisms in the Ascocoryne genus and a reevaluation of myco-diesel production by NRRL 50072. Microbiology pp. mic.0.041327-0 doi:10.1099/mic.0.041327-0.
6. Strobel G, Tomsheck A, Geary B, Spakowicz D, Strobel S, et al. (2010) Endophyte Strain NRRL- 50072 producing volatile organics is a species of Ascocoryne. Mycology: An International Journal on Fungal Biology 1: 187 doi:10.1080/21501203.2010.510122.
7. Strobel GA, Knighton B, Kluck K, Ren Y, Livinghouse T, et al. (2010) The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 156: 3830-3833 doi:10.1099/mic.0.30824-0.
8. Fortman JL, Chhabra S, Mukhopadhyay A, Chou H, Lee TS, et al. (2008) Biofuel alternatives to ethanol: pumping the microbial well. Trends Biotechnol 26: 375-381 doi:10.1016/j.tibtech.2008.03.008.
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.
10. Sukovich DJ, Seffernick JL, Richman JE, Hunt KA, Gralnick JA, et al. (2010) Structure, function, and insights into the biosynthesis of a head-to-head hydrocarbon in Shewanella oneidensis strain MR-1. Appl Environ Microbiol 76: 3842-3849 doi:10.1128/AEM.00433-10.
11. 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.
12. Rude MA, Baron TS, Brubaker S, Alibhai M, Del Cardayre SB, et al. (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.
13. Tressl R, Bahri D, Engel KH, (1981) Lipid oxidation in fruits and vegetables. p. Available: 10.1021/bk-1981-0170.ch016.
14. Tressl R, Bahri D, Engel KH, (1982) Formation of eight-carbon and ten-carbon components in mushrooms (Agaricus campestris). Journal of Agricultural and Food Chemistry 30: 89-93.
15. 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). Biochimica et Biophysica Acta (BBA)-Lipids and Lipid Metabolism 794: 25-30.
16. Wurzenberger M, Grosch W, (1984) Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (psalliota bispora). Biochimica et Biophysica Acta (BBA)- Lipids and Lipid Metabolism 795: 163-165 doi:10.1016/0005-2760(84)90117-6.
17. Brodhun F, Schneider S, Göbel C, Hornung E, Feussner I, (2010) PpoC from Aspergillus nidulans is a fusion protein with only one active haem. Biochem J 425: 553-565 doi:10.1042/BJ20091096.
18. Askenazi M, Driggers EM, Holtzman DA, Norman TC, Iverson S, et al. (2003) Integrating transcriptional and metabolite profiles to direct the engineering of lovastatin-producing fungal strains. Nat Biotech 21: 150-156 doi:10.1038/nbt781.
19. Bradley PH, Brauer MJ, Rabinowitz JD, Troyanskaya OG, (2009) Coordinated concentration changes of transcripts and metabolites in Saccharomyces cerevisiae. PLoS Comput Biol 5: e1000270 doi:10.1371/journal.pcbi.1000270.
20. Redestig H, Costa IG, (2011) Detection and interpretation of metabolite-transcript coresponses using combined profiling data. Bioinformatics 27: i357-i365 doi:10.1093/bioinformatics/btr231.
21. Hirai MY, Yano M, Goodenowe DB, Kanaya S, Kimura T, et al. (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 101: 10205-10210 doi:10.1073/pnas.0403218101.
22. Hancock T, Takigawa I, Mamitsuka H, (2010) Mining metabolic pathways through gene expression. Bioinformatics 26: 2128-2135 doi:10.1093/bioinformatics/btq344.
23. Saito N, Ohashi Y, Soga T, Tomita M, (2010) Unveiling cellular biochemical reactions via metabolomics-driven approaches. Curr Opin Microbiol 13: 358-362 doi:10.1016/j.mib.2010.04.006.
24. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380 doi:10.1038/nature03959.
25. Fitzpatrick D, Logue M, Stajich J, Butler G, (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evolutionary Biology 6: 99 doi:10.1186/1471-2148-6-99.
26. Parra G, Bradnam K, Korf I, (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23: 1061-1067 doi:10.1093/bioinformatics/btm071.
27. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL, (2007) GenBank. Nucleic Acids Research 36: D25-D30 doi:10.1093/nar/gkm929.
28. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, et al. (2008) The Transcriptional Landscape of the Yeast Genome Defined by RNA Sequencing. Science 320: 1344-1349 doi:10.1126/science.1158441.
29. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Meth 5: 621-628 doi:10.1038/nmeth.1226.
30. Supelco Bulletin 869A (n.d.) Solid Phase Microextraction: Solventless Sample Preparation for Monitoring Flavor Compounds by Capillary Gas Chromatography. Available: www.sigmaaldrich.com/etc/medialib/docs/Supelco//4524.pdf.
31. Ozsolak F, Kapranov P, Foissac S, Kim SW, Fishilevich E, et al. (2010) Comprehensive Polyadenylation Site Maps in Yeast and Human Reveal Pervasive Alternative Polyadenylation. Cell 143: 1018-1029 doi:10.1016/j.cell.2010.11.020.
32. Bumgarner SL, Dowell RD, Grisafi P, Gifford DK, Fink GR, (2009) Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. Proceedings of the National Academy of Sciences 106: 18321-18326 doi:10.1073/pnas.0909641106.
33. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, et al. (2010) Integrative Analysis of the Caenorhabditis elegans Genome by the modENCODE Project. Science 330: 1775-1787 doi:10.1126/science.1196914.
34. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238 doi:10.1093/nar/gkn663.
35. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, et al. (2002) Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. European Journal of Biochemistry 269: 4202-4211 doi:10.1046/j.1432-1033.2002.03095.x.
36. Chen X-ai, Ishida N, Todaka N, Nakamura R, Maruyama J-ichi, et al. (2010) Promotion of Efficient Saccharification of Crystalline Cellulose by Aspergillus fumigatus Swo1. Appl Environ Microbiol 76: 2556-2561 doi:10.1128/AEM.02499-09.
37. Fischer CR, Klein-Marcuschamer D, Stephanopoulos G, (2008) Selection and optimization of microbial hosts for biofuels production. Metabolic Engineering 10: 295-304 doi:10.1016/j.ymben.2008.06.009.
38. James EG, Sarah EC, Christina Cuomo LJ, Jennifer RW, Serafim Batzoglou SI, et al. (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105-1115.
39. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, et al. (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nature biotechnology 26: 553-560.
40. Camera SL, Balagué C, Göbel C, Geoffroy P, Legrand M, et al. (2009) The Arabidopsis Patatin-Like Protein 2 (PLP2) Plays an Essential Role in Cell Death Execution and Differentially Affects Biosynthesis of Oxylipins and Resistance to Pathogens. MPMI 22: 469-481 doi:10.1094/MPMI-22-4-0469.
41. Del Sorbo G, Schoonbeek H, De Waard MA, (2000) Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet Biol 30: 1-15.
42. Yadav G, Gokhale RS, Mohanty D, (2009) Towards Prediction of Metabolic Products of Polyketide Synthases: An In Silico Analysis. PLoS Comput Biol 5: e1000351 doi:10.1371/journal.pcbi.1000351.
43. Bouhired S, Weber M, Kempf-Sontag A, Keller NP, Hoffmeister D, (2007) Accurate prediction of the Aspergillus nidulans terrequinone gene cluster boundaries using the transcriptional regulator LaeA. Fungal Genetics and Biology 44: 1134-1145 doi:10.1016/j.fgb.2006.12.010.
44. Yadav G, Gokhale RS, Mohanty D, (2003) SEARCHPKS: a program for detection and analysis of polyketide synthase domains. Nucleic Acids Research 31: 3654-3658 doi:10.1093/nar/gkg607.
45. Piel J, (2010) Biosynthesis of polyketides by trans-AT polyketide synthases. Nat Prod Rep 27: 996-1047 doi:10.1039/b816430b.
46. Koonin EV, Wolf YI, (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Research 36: 6688-6719 doi:10.1093/nar/gkn668.
47. Pellegrini M, Marcotte EM, Thompson MJ, Eisenberg D, Yeates TO, (1999) Assigning protein functions by comparative genome analysis: Protein phylogenetic profiles. Proc Natl Acad Sci U S A 96: 4285-4288.
48. Korbel JO, Jensen LJ, von Mering C, Bork P, (2004) Analysis of genomic context: prediction of functional associations from conserved bidirectionally transcribed gene pairs. Nat Biotech 22: 911-917 doi:10.1038/nbt988.
49. Marcotte EM, Pellegrini M, Ng H-L, Rice DW, Yeates TO, et al. (1999) Detecting Protein Function and Protein-Protein Interactions from Genome Sequences. Science 285: 751-753 doi:10.1126/science.285.5428.751.
50. Overbeek R, Fonstein M, D'Souza M, Pusch GD, Maltsev N, (1999) The use of gene clusters to infer functional coupling. Proceedings of the National Academy of Sciences 96: 2896-2901 doi:10.1073/pnas.96.6.2896.
51. Kumar CG, Everts RE, Loor JJ, Lewin HA, (2010) Functional annotation of novel lineage-specific genes using co-expression and promoter analysis. BMC Genomics 11: 161 doi:10.1186/1471-2164-11-161.
52. Stephanopoulos G, (2007) Challenges in Engineering Microbes for Biofuels Production. Science 315: 801-804 doi:10.1126/science.1139612.
53. Lee SK, Chou H, Ham TS, Lee TS, Keasling JD, (2008) Metabolic engineering of microorganisms for biofuels production: from bugs to synthetic biology to fuels. Current Opinion in Biotechnology 19: 556-563 doi:10.1016/j.copbio.2008.10.014.
54. Andreou A, Brodhun F, Feussner I, (2009) Biosynthesis of oxylipins in non-mammals. Progress in Lipid Research 48: 148-170 doi:10.1016/j.plipres.2009.02.002.
55. Grechkin AN, Hamberg M, (2004) The "heterolytic hydroperoxide lyase" is an isomerase producing a short-lived fatty acid hemiacetal. Biochimica et Biophysica Acta (BBA)- Molecular and Cell Biology of Lipids 1636: 47-58 doi:10.1016/j.bbalip.2003.12.003.
56. Berdy J, (2005) Bioactive Microbial Metabolites. J Antibiot 58: 1-26.
57. Dodds DR, Gross RA, (2007) Chemicals from Biomass. Science 318: 1250-1251 doi:10.1126/science.1146356.
58. Croes D, Couche F, Wodak SJ, van Helden J, (2005) Metabolic PathFinding: inferring relevant pathways in biochemical networks. Nucleic Acids Research 33: W326-W330 doi:10.1093/nar/gki437.
59. Gao J, Ellis LBM, Wackett LP, (2010) The University of Minnesota Biocatalysis/Biodegradation Database: improving public access. Nucleic Acids Res 38: D488-D491 doi:10.1093/nar/gkp771.
60. Moriya Y, Shigemizu D, Hattori M, Tokimatsu T, Kotera M, et al. (2010) PathPred: an enzyme-catalyzed metabolic pathway prediction server. Nucleic Acids Res 38: W138-143 doi:10.1093/nar/gkq318.
61. Rahman SA, Advani P, Schunk R, Schrader R, Schomburg D, (2005) Metabolic pathway analysis web service (Pathway Hunter Tool at CUBIC). Bioinformatics 21: 1189-1193 doi:10.1093/bioinformatics/bti116.
62. Caspi R, Foerster H, Fulcher CA, Kaipa P, Krummenacker M, et al. (2008) The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res 36: D623-D631 doi:10.1093/nar/gkm900.
63. Wink M, (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theoret Appl Genetics 75: 225-233 doi:10.1007/BF00303957.
64. Wieloch W, (2006) Chromosome visualisation in filamentous fungi. J Microbiol Methods 67: 1-8 doi:10.1016/j.mimet.2006.05.022.
65. 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.
66. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410 doi:10.1016/S0022-2836(05)80360-2.
67. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238 doi:10.1093/nar/gkn663.
68. Eddy SR, (2009) A new generation of homology search tools based on probabilistic inference. Genome Inform 23: 205-211.
69. Alam I, Hubbard S, Oliver S, Rattray M, (2007) A kingdom-specific protein domain HMM library for improved annotation of fungal genomes. BMC Genomics 8: 97 doi:10.1186/1471-2164-8-97.
70. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2007) The Pfam protein families database. Nucleic Acids Research 36: D281-D288 doi:10.1093/nar/gkm960.
71. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, et al. (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36: D480-484 doi:10.1093/nar/gkm882.
72. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M, (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182-185 doi:10.1093/nar/gkm321.
73. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29 doi:10.1038/75556.
74. Arnaud MB, Chibucos MC, Costanzo MC, Crabtree J, Inglis DO, et al. (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 doi:10.1093/nar/gkp751.
75. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25 doi:10.1186/gb-2009-10-3-r25.
76. Habegger L, Sboner A, Gianoulis TA, Rozowsky J, Agarwal A, et al. (2010) RSEQtools: A modular framework to analyze RNA-Seq data using compact, anonymized data summaries. Bioinformatics. Available:http://bioinformatics.oxfordjournals.org/content/early/2010/12/05/bioinformatics.btq643.abstract.
77. Kent WJ, (2002) BLAT-the BLAST-like alignment tool. Genome Res 12: 656-664 doi:10.1101/gr.229202.