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Genome Characterization of Oleaginous Aspergillus oryzae BCC7051: A Potential Fungal-Based Platform for Lipid Production

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Abstract

The selected robust fungus, Aspergillus oryzae strain BCC7051 is of interest for biotechnological production of lipid-derived products due to its capability to accumulate high amount of intracellular lipids using various sugars and agro-industrial substrates. Here, we report the genome sequence of the oleaginous A. oryzae BCC7051. The obtained reads were de novo assembled into 25 scaffolds spanning of 38,550,958 bps with predicted 11,456 protein-coding genes. By synteny mapping, a large rearrangement was found in two scaffolds of A. oryzae BCC7051 as compared to the reference RIB40 strain. The genetic relationship between BCC7051 and other strains of A. oryzae in terms of aflatoxin production was investigated, indicating that the A. oryzae BCC7051 was categorized into group 2 nonaflatoxin-producing strain. Moreover, a comparative analysis of the structural genes focusing on the involvement in lipid metabolism among oleaginous yeast and fungi revealed the presence of multiple isoforms of metabolic enzymes responsible for fatty acid synthesis in BCC7051. The alternative routes of acetyl-CoA generation as oleaginous features and malate/citrate/pyruvate shuttle were also identified in this A. oryzae strain. The genome sequence generated in this work is a dedicated resource for expanding genome-wide study of microbial lipids at systems level, and developing the fungal-based platform for production of diversified lipids with commercial relevance.

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References

  1. Ageitos JM, Vallejo JA, Veiga-Crespo P, Villa TG (2011) Oily yeasts as oleaginous cell factories. Appl Microbiol Biotechnol 90:1219–1227

    Article  CAS  PubMed  Google Scholar 

  2. Bhatnagar D, Ehrlich KC, Cleveland TE (2003) Molecular genetic analysis and regulation of aflatoxin biosynthesis. Appl Microbiol Biotechnol 61:83–93

    Article  CAS  PubMed  Google Scholar 

  3. Brown DW, Adams TH, Keller P (1996) Aspergillus has distinct fatty acid synthases for primary and secondary metabolism. Proc Natl Acad Sci USA 93:14873–14877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Cary JW, Wright M, Bhatnagar D, Lee R, Chu FS (1996) Molecular characterization of an Aspergillus parasiticus dehydrogenase gene, norA, located on the aflatoxin biosynthesis gene cluster. Appl Environ Microbiol 62:360–366

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Chang PK, Horn BW, Dorner JW (2005) Sequence breakpoints in the aflatoxin biosynthesis gene cluster and flanking regions in nonaflatoxigenic Aspergillus flavus isolates. Fungal Genet Biol 42:914–923

    Article  CAS  PubMed  Google Scholar 

  6. Coghlan A, Eichler EE, Oliver SG, Paterson AH, Stein L (2005) Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet 21:673–682

    Article  CAS  PubMed  Google Scholar 

  7. Colson I, Delneri D, Oliver SG (2004) Effect of reciprocal chromosomal translocations on the fitness of Saccharomyces cerevisiae. EMBO Rep 5:392–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, Angiuoli S, Bussey H, Bowyer P, Cotty PJ, Dyer PS, Egan A, Galens K, Fraser-Liggett CM, Haas BJ, Inman JM, Kent R, Lemieux S, Malavazi I, Orvis J, Roemer T, Ronning CM, Sundaram JP, Sutton G, Turnrt G, Venter JC, White OR, Whitty BR, Youngman P, Wolfe KH, Goldman GH, Wortman JR, Jiang B, Denning DW, Nierman WC (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4:e1000046

    Article  PubMed  PubMed Central  Google Scholar 

  10. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  11. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acid Res 44:D279–D285

    Article  CAS  PubMed  Google Scholar 

  12. Fischer G, Neuvéglise C, Durrens P, Gaillardin C, Dujon B (2001) Evolution of gene order in the genomes of two related yeast species. Genome Res 11:2009–2019

    Article  CAS  PubMed  Google Scholar 

  13. Fraser JA, Huang JC, Pukkila-Worley R, Alspaugh A, Mitchell TG, Heitman J (2005) Chromosomal translocation and segmental duplication in Cryptococcus neoformans. Eukaryot Cell 4:401–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Galperin MY, Makarova KS, Wolf YI, Koonin EV (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acid Res 43:D261–D269

    Article  CAS  PubMed  Google Scholar 

  15. Haft DH, Selengut JD, Ritchter RA, Harkins D, Basu MK, Beck E (2013) TIGRFAMs and genome properties in 2013. Nucleic Acid Res 41:D387–D395

    Article  CAS  PubMed  Google Scholar 

  16. Kiyota T, Hamada R, Sakamoto K, Iwashita K, Yamada O, Mikami S (2011) Aflatoxin non-productivity of Aspergillus oryzae caused by loss of function in the aflJ gene product. J Biosci Bioeng 111:512–517

    Article  CAS  PubMed  Google Scholar 

  17. Kobayashi T, Abe K, Asai K, Gomi K, Juvvadi PR, Kato M, Kitamoto K, Takeuchi M, Machida M (2007) Genomics of Aspergillus oryzae. Biosci Biotechnol Biochem 71:646–670

    Article  CAS  PubMed  Google Scholar 

  18. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kusumoto K, Yabe K, Nogata Y, Ohta H (1998) Transcript of a homolog of aflR, a regulatory gene for aflatoxin synthesis in Aspergillus parasiticus, was not detected in Aspergillus oryzae strains. FEMS Microbiol Lett 169:303–307

    Article  CAS  PubMed  Google Scholar 

  20. Kusumoto K, Nogata Y, Ohta H (2000) Directed deletions in the aflatoxin biosynthesis gene homolog cluster of Aspergillus oryzae. Curr Genet 37:104–111

    Article  CAS  PubMed  Google Scholar 

  21. Lee YH, Tominaga M, Hayashi R, Sakamoto K, Yamada O, Akita O (2006) Aspergillus oryzae strains with a large deletion of the aflatoxin biosynthetic homologous gene cluster differentiated by chromosomal breakage. Appl Microbiol Biotechnol 72:339–345

    Article  CAS  PubMed  Google Scholar 

  22. Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acid Res 43:D257–D260

    Article  CAS  PubMed  Google Scholar 

  23. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Juvvadi PR, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161

    Article  PubMed  Google Scholar 

  24. Marchler-Bauer A, Anderson JB, DeWeese-Scott C, Fedorova ND, Geer LY, He S, Hurwitz DI, Jackson JD, Jacobs AR, Lanczycki CJ, Liebert CA, Liu C, Madej T, Marchler GH, Mazumder R, Nikolskaya AN, Panchenko AR, Rao BS, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Vasudevan S, Wang Y, Yamashita RA, Yin JJ, Bryant SH (2003) CDD: a curated Entrez database of conserved domain alignments. Nucleic Acid Res 31:383–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD: NCBI’s conserved domain database. Nucleic Acid Res 43:D222–D226

    Article  CAS  PubMed  Google Scholar 

  26. Mario S, Mark D, Robert B, David H (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24:637–644

    Article  Google Scholar 

  27. Meng X, Yang J, Xu X, Zhang L, Nie Q, Xian M (2009) Biodiesel production from oleaginous microorganisms. Renew Energy 34:1–5

    Article  Google Scholar 

  28. Morita T, Koike H, Hagiwara H, Ito E, Machida M, Sato S, Have H, Kitamoto D (2014) Genome and transcriptome analysis of the Basidiomycetous yeast Pseudozyma antarctica producing extracellular glycolipids, mannosylerythritol lipids. PLoS ONE 9(2):e86490

    Article  PubMed  PubMed Central  Google Scholar 

  29. Pérez-Ortín JE, Querol A, Puig S, Barrio E (2002) Molecular characterization of chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res 12:1533–1539

    Article  PubMed  PubMed Central  Google Scholar 

  30. Pietrocola F, Galluzzi L, Bravo-San Pedro JM, Madeo F, Kroemer G (2015) Acetyl-coenzyme A: a central metabolite and second messenger. Cell Metab 21:805–821

    Article  CAS  PubMed  Google Scholar 

  31. Ratledge C (1991) Microorganisms for lipids. Acta Biotechnol 11:429–438

    Article  CAS  Google Scholar 

  32. Ratledge C (2002) Regulation of lipid accumulation in oleaginous micro-organisms. Biochem Soc Trans 30:1047–1050

    Article  CAS  PubMed  Google Scholar 

  33. Ruenwai R, Cheevadhanarak S, Rachdawong S, Tanticharoen M, Laoteng K (2010) Oxygen-induced expression of Δ6-, Δ9- and Δ12-desaturase genes modulate fatty acid composition in Mucor rouxii. Appl Microbiol Biotechnol 86:327–334

    Article  CAS  PubMed  Google Scholar 

  34. Shin GH, Veen M, Stahl U, Lang C (2012) Overexpression of genes of the fatty acid biosynthesis pathway leads to accumulation of sterols in Saccharomyces cerevisiae. Yeast 29:371–383

    Article  CAS  PubMed  Google Scholar 

  35. Soderlund C, Bomhoff M, Nelson WM (2011) Symap v3.4: 2 turnkey synteny system with application to plant genomes. Nucleic Acid Res 39:e68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Stanke M, Diekhans M, Baertsch R, Haussler D (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24:637–644

    Article  CAS  PubMed  Google Scholar 

  37. Takeda I, Tamano K, Yamane N, Ishii T, Miura A, Umemura M, Terai G, Baker SE, Koike H, Machida M (2014) Genome sequence of the Mucoromycotina fungus Umbelopsis isabellina, an effective producer of lipids. Genome Announc. doi:10.1128/genomeA.00071-14

    Google Scholar 

  38. Tamano K, Bruno KS, Karagiosis SA, Culley DE, Deng S, Collett JR, Umemura M, Koike H, Baker SE, Machida M (2013) Increased production of fatty acids and triacylglycerides in Aspergillus oryzae by enhancing expressions of fatty acid synthesis-related genes. Appl Genet Mol Biotechnol 97:269–281

    CAS  Google Scholar 

  39. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2003) The COG database: an updated version includes eukaryotes. BMC Bioinform 4:41

    Article  Google Scholar 

  41. Tominaga M, Lee YH, Hayashi R, Suzuki Y, Yamada O, Sakamoto K, Gotoh K, Akita O (2006) Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains. Appl Microbiol Biotechnol 72:484–490

    CAS  Google Scholar 

  42. Vongsangnak W, Olsen P, Hansen K, Krogsgaard S, Nielsen J (2008) Improved annotation through genome-scale metabolic modeling of Aspergillus oryzae. BMC Genomics 9:245

    Article  PubMed  PubMed Central  Google Scholar 

  43. Vongsangnak W, Ruenwai R, Tang X, Hu X, Zhang H, Shen B, Song Y, Laoteng K (2013) Genome-scale analysis of the metabolic networks of oleaginous Zygomycete fungi. Gene 521:180–190

    Article  CAS  PubMed  Google Scholar 

  44. Vorapreeda T, Thammarongtham C, Cheevadhanarak S, Laoteng K (2012) Alternative routes of acetyl-CoA synthesis identified by comparative genomic analysis: involvement in the lipid production of oleaginous yeast and fungi. Microbiology 158:217–228

    Article  CAS  PubMed  Google Scholar 

  45. Wynn JP, Hamid AA, Li Y, Ratledge C (2001) Biochemical events leading to the diversion of carbon into storage lipids in the oleaginous fungi Mucor circinelloides and Mortierella alpina. Microbiology 147:2857–2864

    Article  CAS  PubMed  Google Scholar 

  46. Yu J (2012) Current understanding on aflatoxin biosynthesis and future perspective in reducing aflatoxin contamination. Toxins 4:1024–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zhang Y, Min Q, Xu J, Zhang K, Chen S, Wang H, Li D (2016) Effect of malate on docosahexaenoic acid production from Schizochytrium sp. B4D1. Electronic J Biotechnol 19:56–60

    Article  CAS  Google Scholar 

  48. Zhao L, Cánovas-Márquez JT, Tang X, Chen H, Chen YQ, Chen W, Garre V, Song V, Ratledge C (2016) Role of malate transporter in lipid accumulation of oleaginous fungus Mucor circinelloides. Appl Microbiol Biotechnol 100:1297–1305

    Article  CAS  PubMed  Google Scholar 

  49. Zhu Z, Zhang S, Liu H, Shen H, Lin X, Yang F, Zhou YJ, Jin G, Ye M, Zou H, Zhao ZK (2012) A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat Commun 3:1112

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We gratefully thank Uppsala Genome Center for Pacific BioScience platform sequencing service. We also thank Comparative Genomics Group, Division of BioScience, Oak Ridge National Laboratory for computational resources for gene prediction.

Funding

This work was financially supported by National Center for Genetic Engineering and Biotechnology (Project No. P-14-50613). The Swedish Research Council (VR-2013-4504) is acknowledged for financial support of Intawat Nookaew and sequencing.

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Correspondence to Kobkul Laoteng.

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Thammarongtham, C., Nookaew, I., Vorapreeda, T. et al. Genome Characterization of Oleaginous Aspergillus oryzae BCC7051: A Potential Fungal-Based Platform for Lipid Production. Curr Microbiol 75, 57–70 (2018). https://doi.org/10.1007/s00284-017-1350-7

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