Genome characterization of the oleaginous fungus mortierella alpina

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Wang, Lei ^b,c   Chen, Wei ^a   Feng, Yun ^b,c   Ren, Yan ^b   Gu, Zhennan ^d   Chen, Haiqin ^a,d   Wang, Hongchao ^a   Thomas, Michael J ^d   Zhang, Baixi ^a   Berquin, Isabelle M ^d   Li, Yang ^b   Wu, Jiansheng ^d   Zhang, Huanxin ^b   Song, Yuanda ^a   Liu, Xiang ^e   Norris, James S ^e   Wang, Suriguga ^b   Du, Peng ^f   Shen, Junguo ^f   Wang, Na ^f   Yang, Yanlin ^f   Wang, Wei ^b   Feng, Lu ^b,c   Ratledge, Colin ^g   Zhang, Hao ^a   Chen, Yong Q ^d   more..

^a JIANGNAN UNIVERSITY   (China)

^b NANKAI UNIVERSITY   (China)

^c Tianjin Research Center for Functional Genomics and Biochip   (China)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

^e MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^f Tianjin Biochip Corporation   (China)

^g UNIVERSITY OF HULL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

24(28) METHYLENECHOLESTEROL; ACETYL COENZYME A; CHOLESTEROL DERIVATIVE; DESMOSTEROL; FATTY ACID SYNTHASE; GENOMIC DNA; GLYCEROLIPID; GLYCEROPHOSPHOLIPID; MALONYL COENZYME A; SPHINGOLIPID; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; FATTY ACID; FUNGAL PROTEIN; LIPID;

ARTICLE; ASCOMYCETES; BASIDIOMYCETES; CHYTRIDIOMYCETES; CONTROLLED STUDY; EUMYCOTA; FATTY ACID SYNTHESIS; FUNGAL GENE; FUNGAL GENOME; GENE DUPLICATION; GENE FUNCTION; GENE MAPPING; GENETIC ENGINEERING; GENOME ANALYSIS; GENOME SIZE; HIGH THROUGHPUT SEQUENCING; LIPASE GENE; LIPID ANALYSIS; LIPID METABOLISM; LIPOGENESIS; MOLECULAR EVOLUTION; MORTIERELLA ALPINA; MUCOROMYCOTA; MULTIGENE FAMILY; NONHUMAN; PHYLOGENY; SIGNAL TRANSDUCTION; ASEXUAL REPRODUCTION; CHEMISTRY; CHROMOSOME MAP; GENETICS; METABOLISM; MITOCHONDRIAL GENOME; MORTIERELLA; PROTEIN TERTIARY STRUCTURE; STAINING;

CHROMOSOME MAPPING; FATTY ACIDS; FUNGAL PROTEINS; GENOME, FUNGAL; GENOME, MITOCHONDRIAL; LIPIDS; LIPOGENESIS; MORTIERELLA; MULTIGENE FAMILY; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; REPRODUCTION, ASEXUAL; STAINING AND LABELING;

EID: 82955201624     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028319     Document Type: Article

References (94)

1. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, et al. (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111: 509-547.
2. Bajpai PK, Bajpai P, Ward OP, (1991) Arachidonic Acid Production by Fungi. Appl Environ Microbiol 57: 1255-1258.
3. Ratledge C, Wynn JP, (2002) The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol 51: 1-51.
4. Ho SY, Jiang Y, Chen F, (2007) Polyunsaturated fatty acids (PUFAs) content of the fungus Mortierella alpina isolated from soil. J Agric Food Chem 55: 3960-3966.
5. Jang HD, Lin YY, Yang SS, (2005) Effect of culture media and conditions on polyunsaturated fatty acids production by Mortierella alpina. Bioresour Technol 96: 1633-1644.
6. Ratledge C, (2004) Fatty acid biosynthesis in microorganisms being used for Single Cell Oil production. Biochimie 86: 807-815.
7. Burns RA, Wibert GJ, Diersen-Schade DA, Kelly CM, (1999) Evaluation of single-cell sources of docosahexaenoic acid and arachidonic acid: 3-month rat oral safety study with an in utero phase. Food Chem Toxicol 37: 23-36.
8. Streekstra H, (1997) On the safety of Mortierella alpina for the production of food ingredients, such as arachidonic acid. J Biotechnol 56: 153-165.
9. Hempenius RA, Lina BA, Haggitt RC, (2000) Evaluation of a subchronic (13-week) oral toxicity study, preceded by an in utero exposure phase, with arachidonic acid oil derived from Mortierella alpina in rats. Food Chem Toxicol 38: 127-139.
10. Simopoulos AP, (1999) Essential fatty acids in health and chronic disease. Am J Clin Nutr 70: 560S-569S.
11. Berquin IM, Edwards IJ, Chen YQ, (2008) Multi-targeted therapy of cancer by omega-3 fatty acids. Cancer Lett 269: 363-377.
12. Chen YQ, Edwards IJ, Kridel SJ, Thornburg T, Berquin IM, (2007) Dietary fat-gene interactions in cancer. Cancer Metastasis Rev 26: 535-551.
13. Michaelson LV, Lazarus CM, Griffiths G, Napier JA, Stobart AK, (1998) Isolation of a Delta5-fatty acid desaturase gene from Mortierella alpina. J Biol Chem 273: 19055-19059.
14. Sakuradani E, Kobayashi M, Shimizu S, (1999) Delta6-fatty acid desaturase from an arachidonic acid-producing Mortierella fungus. Gene cloning and its heterologous expression in a fungus, Aspergillus. Gene 238: 445-453.
15. Sakuradani E, Kobayashi M, Shimizu S, (1999) Delta 9-fatty acid desaturase from arachidonic acid-producing fungus. Unique gene sequence and its heterologous expression in a fungus, Aspergillus. Eur J Biochem 260: 208-216.
16. Sakuradani E, Kobayashi M, Ashikari T, Shimizu S, (1999) Identification of Delta12-fatty acid desaturase from arachidonic acid-producing mortierella fungus by heterologous expression in the yeast Saccharomyces cerevisiae and the fungus Aspergillus oryzae. Eur J Biochem 261: 812-820.
17. Sakuradani E, Abe T, Iguchi K, Shimizu S, (2005) A novel fungal omega3-desaturase with wide substrate specificity from arachidonic acid-producing Mortierella alpina 1S-4. Appl Microbiol Biotechnol 66: 648-654.
18. Ratledge C, (2002) Regulation of lipid accumulation in oleaginous micro-organisms. Biochem Soc Trans 30: 1047-1050.
19. Seif E, Leigh J, Liu Y, Roewer I, Forget L, et al. (2005) Comparative mitochondrial genomics in zygomycetes: bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms. Nucleic Acids Res 33: 734-744.
20. Zhang Y, Adams IP, Ratledge C, (2007) Malic enzyme: the controlling activity for lipid production? Overexpression of malic enzyme in Mucor circinelloides leads to a 2.5-fold increase in lipid accumulation. Microbiology 153: 2013-2025.
21. Zhang Y, Ratledge C, (2008) Multiple isoforms of malic enzyme in the oleaginous fungus, Mortierella alpina. Mycol Res 112: 725-730.
22. Li Y, Adams IP, Wynn JP, Ratledge C, (2005) Cloning and characterization of a gene encoding a malic enzyme involved in anaerobic growth in Mucor circinelloides. Mycol Res 109: 461-468.
23. Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, et al. (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29: 22-28.
24. Cresnar B, Petric S, (2011) Cytochrome P450 enzymes in the fungal kingdom. Biochim Biophys Acta 1814: 29-35.
25. Leibundgut M, Maier T, Jenni S, Ban N, (2008) The multienzyme architecture of eukaryotic fatty acid synthases. Curr Opin Struct Biol 18: 714-725.
26. White SW, Zheng J, Zhang YM, Rock CO, (2005) The structural biology of type II fatty acid biosynthesis. Annu Rev Biochem 74: 791-831.
27. Maier T, Jenni S, Ban N, (2006) Architecture of mammalian fatty acid synthase at 4.5 A resolution. Science 311: 1258-1262.
28. Maier T, Leibundgut M, Ban N, (2008) The Crystal Structure of a Mammalian Fatty Acid Synthase. Science 321: 1315-1322.
29. Jenni S, Leibundgut M, Maier T, Ban N, (2006) Architecture of a fungal fatty acid synthase at 5 A resolution. Science 311: 1263-1267.
30. Jenni S, Leibundgut M, Boehringer D, Frick C, Mikolasek B, et al. (2007) Structure of fungal fatty acid synthase and implications for iterative substrate shuttling. Science 316: 254-261.
31. Lomakin IB, Xiong Y, Steitz TA, (2007) The crystal structure of yeast fatty acid synthase, a cellular machine with eight active sites working together. Cell 129: 319-332.
32. Ando A, Sumida Y, Negoro H, Suroto DA, Ogawa J, et al. (2009) Establishment of Agrobacterium tumefaciens-mediated transformation of an oleaginous fungus, Mortierella alpina 1S-4, and its application for eicosapentaenoic acid producer breeding. Appl Environ Microbiol 75: 5529-5535.
33. Sakuradani E, Shimizu S, (2009) Single cell oil production by Mortierella alpina. J Biotechnol 144: 31-36.
34. Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, et al. (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5: e1000549.
35. Murray MG, Thompson WF, (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8: 4321-4325.
36. 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.
37. Goldberg SM, Johnson J, Busam D, Feldblyum T, Ferriera S, et al. (2006) A Sanger/pyrosequencing hybrid approach for the generation of high-quality draft assemblies of marine microbial genomes. Proc Natl Acad Sci U S A 103: 11240-11245.
38. Gordon D, Desmarais C, Green P, (2001) Automated finishing with autofinish. Genome Res 11: 614-625.
39. Stanke M, Waack S, (2003) Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19 (Suppl 2): ii215-225.
40. Majoros WH, Pertea M, Salzberg SL, (2004) TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20: 2878-2879.
41. Korf I, (2004) Gene finding in novel genomes. BMC Bioinformatics 5: 59.
42. 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.
43. Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, et al. (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol 9: R7.
44. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
45. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
46. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M, (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32: D277-280.
47. Wu CH, Apweiler R, Bairoch A, Natale DA, Barker WC, et al. (2006) The Universal Protein Resource (UniProt): an expanding universe of protein information. Nucleic Acids Res 34: D187-191.
48. Chang A, Scheer M, Grote A, Schomburg I, Schomburg D, (2009) BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res 37: D588-592.
49. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, et al. (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33: W116-120.
50. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, et al. (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34: D247-251.
51. Attwood TK, Bradley P, Flower DR, Gaulton A, Maudling N, et al. (2003) PRINTS and its automatic supplement, prePRINTS. Nucleic Acids Res 31: 400-402.
52. Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, et al. (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34: D257-260.
53. Hulo N, Bairoch A, Bulliard V, Cerutti L, De Castro E, et al. (2006) The PROSITE database. Nucleic Acids Res 34: D227-230.
54. Haft DH, Selengut JD, White O, (2003) The TIGRFAMs database of protein families. Nucleic Acids Res 31: 371-373.
55. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, et al. (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13: 2129-2141.
56. Li L, Stoeckert CJ Jr, Roos DS, (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
57. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, et al. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110: 462-467.
58. Lowe TM, Eddy SR, (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
59. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, et al. (2005) Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33: D121-124.
60. Braun BR, van Het Hoog M, d'Enfert C, Martchenko M, Dungan J, et al. (2005) A human-curated annotation of the Candida albicans genome. PLoS Genet 1: 36-57.
61. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, et al. (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438: 1151-1156.
62. Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, et al. (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4: e1000046.
63. Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, et al. (2004) The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304: 304-307.
64. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, et al. (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105-1115.
65. Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, et al. (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25: 221-231.
66. Andersen MR, Salazar MP, Schaap PJ, van de Vondervoort PJ, Culley D, et al. (2011) Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88. Genome Res 21: 885-897.
67. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, et al. (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438: 1157-1161.
68. Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, et al. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230.
69. Thatcher LF, Gardiner DM, Kazan K, Manners J, (2011) A Highly Conserved Effector in Fusarium oxysporum is Required for Full Virulence on Arabidopsis. Mol Plant Microbe Interact.
70. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, et al. (2004) Genome evolution in yeasts. Nature 430: 35-44.
71. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, et al. (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307: 1321-1324.
72. Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG, et al. (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400-1402.
73. Martin F, Aerts A, Ahren D, Brun A, Danchin EG, et al. (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88-92.
74. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, et al. (2007) Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci U S A 104: 18730-18735.
75. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, et al. (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980-986.
76. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, et al. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868.
77. Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, et al. (2008) The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 9: R77.
78. Jeffries TW, Grigoriev IV, Grimwood J, Laplaza JM, Aerts A, et al. (2007) Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis. Nat Biotechnol 25: 319-326.
79. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, et al. (1996) Life with 6000 genes. Science 274: 546, 563-547.
80. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415: 871-880.
81. Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
82. Scannell DR, Frank AC, Conant GC, Byrne KP, Woolfit M, et al. (2007) Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication. Proc Natl Acad Sci U S A 104: 8397-8402.
83. Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, et al. (2011) Comparative functional genomics of the fission yeasts. Science 332: 930-936.
84. Chaisson MJ, Brinza D, Pevzner PA, (2009) De novo fragment assembly with short mate-paired reads: Does the read length matter? Genome Res 19: 336-346.
85. Zerbino DR, Birney E, (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
86. Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, et al. (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 31: 5654-5666.
87. Bligh EG, Dyer WJ, (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
88. Metcalfe LD, Schmitz AA, Pelka JR, (1966) Rapid preparation of fatty acids esters from lipids for gas chromatographic analysis. Analytical Chemistry 38: 514-515.
89. Carr TP, Andresen CJ, Rudel LL, (1993) Enzymatic determination of triglyceride, free cholesterol, and total cholesterol in tissue lipid extracts. Clin Biochem 26: 39-42.
90. Rouser G, Siakotos AN, Fleischer S, (1966) Quantitative analysis of phospholipids by thin-layer chromatography and phosphorus analysis of spots. Lipids 1: 85-86.
91. Van Kessel WS, Hax WM, Demel RA, De Gier J, (1977) High performance liquid chromatographic separation and direct ultraviolet detection of phospholipids. Biochim Biophys Acta 486: 524-530.
92. Brugger B, Erben G, Sandhoff R, Wieland FT, Lehmann WD, (1997) Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc Natl Acad Sci U S A 94: 2339-2344.
93. Pettus BJ, Kroesen BJ, Szulc ZM, Bielawska A, Bielawski J, et al. (2004) Quantitative measurement of different ceramide species from crude cellular extracts by normal-phase high-performance liquid chromatography coupled to atmospheric pressure ionization mass spectrometry. Rapid Commun Mass Spectrom 18: 577-583.
94. Bielawski J, Szulc ZM, Hannun YA, Bielawska A, (2006) Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39: 82-91.