1887

Abstract

For a bio-based economy, microbial lipids offer a potential solution as alternative feedstocks in the oleochemical industry. The existing genome data for the promising strains, oleaginous yeasts and fungi, allowed us to investigate candidate orthologous sequences that participate in their oleaginicity. Comparative genome analysis of the non-oleaginous (, and ) and oleaginous strains (, , and ) showed that 209 orthologous protein sequences of the oleaginous microbes were distributed over several processes of the cells. Based on the 41 sequences categorized by metabolism, putative routes potentially involved in the generation of precursors for fatty acid and lipid synthesis, particularly acetyl-CoA, were then identified that were not present in the non-oleaginous strains. We found a set of the orthologous oleaginous proteins that was responsible for the biosynthesis of this key two-carbon metabolite through citrate catabolism, fatty acid β-oxidation, leucine metabolism and lysine degradation. Our findings suggest a relationship between carbohydrate, lipid and amino acid metabolism in the biosynthesis of acetyl-CoA, which contributes to the lipid production of oleaginous microbes.

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2012-01-01
2022-01-19
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References

  1. Ageitos J. M., Vallejo J. A., Veiga-Crespo P., Villa T. G. ( 2011). Oily yeasts as oleaginous cell factories. Appl Microbiol Biotechnol 90:1219–1227 [View Article][PubMed]
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. ( 1997). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [View Article][PubMed]
    [Google Scholar]
  3. Athenstaedt K., Jolivet P., Boulard C., Zivy M., Negroni L., Nicaud J. M., Chardot T. ( 2006). Lipid particle composition of the yeast Yarrowia lipolytica depends on the carbon source. Proteomics 6:1450–1459 [View Article][PubMed]
    [Google Scholar]
  4. Beopoulos A., Mrozova Z., Thevenieau F., Le Dall M. T., Hapala I., Papanikolaou S., Chardot T., Nicaud J. M. ( 2008). Control of lipid accumulation in the yeast Yarrowia lipolytica. . Appl Environ Microbiol 74:7779–7789 [View Article][PubMed]
    [Google Scholar]
  5. Beopoulos A., Cescut J., Haddouche R., Uribelarrea J. L., Molina-Jouve C., Nicaud J. M. ( 2009). Yarrowia lipolytica as a model for bio-oil production. Prog Lipid Res 48:375–387 [View Article][PubMed]
    [Google Scholar]
  6. Beopoulos A., Nicaud J. M., Gaillardin C. ( 2011). An overview of lipid metabolism in yeasts and its impact on biotechnological processes. Appl Microbiol Biotechnol 90:1193–1206 [View Article][PubMed]
    [Google Scholar]
  7. Certik M., Megova J., Horenitzky R. ( 1999). Effect of nitrogen sources on the activities of lipogenic enzymes in oleaginous fungus Cunninghamella echinulata. . J Gen Appl Microbiol 45:289–293 [View Article][PubMed]
    [Google Scholar]
  8. Claros M. G., Vincens P. ( 1996). Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241:779–786 [View Article][PubMed]
    [Google Scholar]
  9. Courchesne N. M. D., Parisien A., Wang B., Lan C. Q. ( 2009). Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. J Biotechnol 141:31–41 [View Article][PubMed]
    [Google Scholar]
  10. Daum G., Wagner A., Czabany T., Athenstaedt K. ( 2007). Dynamics of neutral lipid storage and mobilization in yeast. Biochimie 89:243–248 [View Article][PubMed]
    [Google Scholar]
  11. Dietrich F. S., Voegeli S., Brachat S., Lerch A., Gates K., Steiner S., Mohr C., Pöhlmann R., Luedi P. & other authors ( 2004). The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304:304–307 [View Article][PubMed]
    [Google Scholar]
  12. Dobson R. C., Griffin M. D., Roberts S. J., Gerrard J. A. ( 2004). Dihydrodipicolinate synthase (DHDPS) from Escherichia coli displays partial mixed inhibition with respect to its first substrate, pyruvate. Biochimie 86:311–315 [View Article][PubMed]
    [Google Scholar]
  13. Dobson P. D., Smallbone K., Jameson D., Simeonidis E., Lanthaler K., Pir P., Lu C., Swainston N., Dunn W. B. & other authors ( 2010). Further developments towards a genome-scale metabolic model of yeast. BMC Syst Biol 4:145 [View Article][PubMed]
    [Google Scholar]
  14. Dulermo T., Nicaud J. M. ( 2011). Involvement of the G3P shuttle and β-oxidation pathway in the control of TAG synthesis and lipid accumulation in Yarrowia lipolytica. . Metab Eng 13:482–491 [View Article][PubMed]
    [Google Scholar]
  15. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. ( 2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016 [View Article][PubMed]
    [Google Scholar]
  16. Finn R. D., Mistry J., Tate J., Coggill P., Heger A., Pollington J. E., Gavin O. L., Gunasekaran P., Ceric G. & other authors ( 2010). The Pfam protein families database. Nucleic Acids Res 38:Database issueD211–D222 [View Article][PubMed]
    [Google Scholar]
  17. Goffeau A., Barrell B. G., Bussey H., Davis R. W., Dujon B., Feldmann H., Galibert F., Hoheisel J. D., Jacq C. & other authors ( 1996). Life with 6000 genes. Science 274:546–567 [View Article][PubMed]
    [Google Scholar]
  18. Harris M. A., Clark J., Ireland A., Lomax J., Ashburner M., Foulger R., Eilbeck K., Lewis S., Marshall B. Gene Ontology Consortium ( 2004). The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:Database issueD258–D261 [View Article][PubMed]
    [Google Scholar]
  19. Harris R. A., Joshi M., Jeoung N. H., Obayashi M. ( 2005). Overview of the molecular and biochemical basis of branched-chain amino acid catabolism. J Nutr 135:Suppl.1527S–1530S[PubMed]
    [Google Scholar]
  20. Jones D. T., Taylor W. R., Thornton J. M. ( 1992). The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282[PubMed]
    [Google Scholar]
  21. Jones T., Federspiel N. A., Chibana H., Dungan J., Kalman S., Magee B. B., Newport G., Thorstenson Y. R., Agabian N. & other authors ( 2004). The diploid genome sequence of Candida albicans. . Proc Natl Acad Sci U S A 101:7329–7334 [View Article][PubMed]
    [Google Scholar]
  22. Kamisaka Y., Tomita N., Kimura K., Kainou K., Uemura H. ( 2007). DGA1 (diacylglycerol acyltransferase gene) overexpression and leucine biosynthesis significantly increase lipid accumulation in the Δsnf2 disruptant of Saccharomyces cerevisiae . Biochem J 408:61–68 [View Article][PubMed]
    [Google Scholar]
  23. Kanehisa M., Goto S., Kawashima S., Okuno Y., Hattori M. ( 2004). The KEGG resource for deciphering the genome. Nucleic Acids Res 32:Database issueD277–D280 [View Article][PubMed]
    [Google Scholar]
  24. Katoh K., Toh H. ( 2008). Recent developments in the mafft multiple sequence alignment program. Brief Bioinform 9:286–298 [View Article][PubMed]
    [Google Scholar]
  25. Kaur P., Worgan J. T. ( 1982). Lipid production by Aspergillus oryzae from starch substrates. Eur J Appl Microbiol Biotechnol 16:126–130 [View Article]
    [Google Scholar]
  26. Laoteng K., Čertik M., Cheevadhanarak S. ( 2011). Mechanisms controlling lipid accumulation and polyunsaturated fatty acid synthesis in oleaginous fungi. Chem Pap 65:97–103 [View Article]
    [Google Scholar]
  27. Lin H., Cheng W., Ding H. T., Chen X. J., Zhou Q. F., Zhao Y. H. ( 2010). Direct microbial conversion of wheat straw into lipid by a cellulolytic fungus of Aspergillus oryzae A-4 in solid-state fermentation. Bioresour Technol 101:7556–7562 [View Article][PubMed]
    [Google Scholar]
  28. Liu B., Zhao Z. ( 2007). Biodiesel production by direct methanolysis of oleaginous microbial biomass. J Chem Technol Biotechnol 82:775–780 [View Article]
    [Google Scholar]
  29. Ma L. J., Ibrahim A. S., Skory C., Grabherr M. G., Burger G., Butler M., Elias M., Idnurm A., Lang B. F. & other authors ( 2009). Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5:e1000549 [View Article][PubMed]
    [Google Scholar]
  30. Machida M., Asai K., Sano M., Tanaka T., Kumagai T., Terai G., Kusumoto K., Arima T., Akita O. & other authors ( 2005). Genome sequencing and analysis of Aspergillus oryzae. . Nature 438:1157–1161 [View Article][PubMed]
    [Google Scholar]
  31. Meng X., Yang J., Xu X., Zhang L., Nie Q., Xian M. ( 2009). Biodiesel production from oleaginous microorganisms. Renew Energy 34:1–5 [View Article]
    [Google Scholar]
  32. Neuberger G., Maurer-Stroh S., Eisenhaber B., Hartig A., Eisenhaber F. ( 2003). Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J Mol Biol 328:567–579 [View Article][PubMed]
    [Google Scholar]
  33. Nookaew I., Jewett M. C., Meechai A., Thammarongtham C., Laoteng K., Cheevadhanarak S., Nielsen J., Bhumiratana S. ( 2008). The genome-scale metabolic model iIN800 of Saccharomyces cerevisiae and its validation: a scaffold to query lipid metabolism. BMC Syst Biol 2:71 [View Article][PubMed]
    [Google Scholar]
  34. Oliver D. J., Nikolau B. J., Wurtele E. S. ( 2009). Acetyl-CoA – life at the metabolic nexus. Plant Sci 176:597–601 [View Article]
    [Google Scholar]
  35. Picataggio S., Rohrer T., Deanda K., Lanning D., Reynolds R., Mielenz J., Eirich L. D. ( 1992). Metabolic engineering of Candida tropicalis for the production of long-chain dicarboxylic acids. Biotechnology (N Y) 10:894–898 [View Article][PubMed]
    [Google Scholar]
  36. Ratledge C. ( 1986). The potential of microorganisms for oil production – a review of recent publications. Proceedings of World Conference on Emerging Technologies in the Fats and Oils Industry318–330 Baldwin A. R. Champaign, IL: American Oil Chemists’ Society;
    [Google Scholar]
  37. Ratledge C. ( 2002). Regulation of lipid accumulation in oleaginous micro-organisms. Biochem Soc Trans 30:1047–1050 [View Article][PubMed]
    [Google Scholar]
  38. Ratledge C. ( 2004). Fatty acid biosynthesis in microorganisms being used for Single Cell Oil production. Biochimie 86:807–815 [View Article][PubMed]
    [Google Scholar]
  39. Ratledge C., Wynn J. P. ( 2002). The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol 51:1–51 [View Article][PubMed]
    [Google Scholar]
  40. Ruenwai R., Cheevadhanarak S., Laoteng K. ( 2009). Overexpression of acetyl-CoA carboxylase gene of Mucor rouxii enhanced fatty acid content in Hansenula polymorpha. . Mol Biotechnol 42:327–332 [View Article][PubMed]
    [Google Scholar]
  41. Ruenwai R., Cheevadhanarak S., Rachdawong S., Tanticharoen M., Laoteng K. ( 2010). Oxygen-induced expression of Δ6-, Δ9- and Δ12-desaturase genes modulates fatty acid composition and lipid content in Mucor rouxii . Appl Microbiol Biotechnol 86:327–334 [View Article][PubMed]
    [Google Scholar]
  42. Saitou N., Nei M. ( 1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  43. Santos-Fo F., Fill T. P., Nakamura J., Monteiro M. R., Rodrigues-Fo E. ( 2011). Endophytic fungi as a source of biofuel precursors. J Microbiol Biotechnol 21:728–733 [View Article][PubMed]
    [Google Scholar]
  44. Schulz H. ( 1996). Oxidation of fatty acids. Biochemistry of Lipids, Lipoproteins and Membranes75–99 Vance D. E., Vance J. E. Amsterdam: Elsevier Science; [View Article]
    [Google Scholar]
  45. Shen Y. Q., Burger G. ( 2009). Plasticity of a key metabolic pathway in fungi. Funct Integr Genomics 9:145–151 [View Article][PubMed]
    [Google Scholar]
  46. Sherman D. J., Martin T., Nikolski M., Cayla C., Souciet J. L., Durrens P. Génolevures Consortium ( 2009). Génolevures: protein families and synteny among complete hemiascomycetous yeast proteomes and genomes. Nucleic Acids Res 37:Database issueD550–D554 [View Article][PubMed]
    [Google Scholar]
  47. Song Y., Wynn J. P., Li Y., Grantham D., Ratledge C. ( 2001). A pre-genetic study of the isoforms of malic enzyme associated with lipid accumulation in Mucor circinelloides. . Microbiology 147:1507–1515[PubMed]
    [Google Scholar]
  48. Strijbis K., Distel B. ( 2010). Intracellular acetyl unit transport in fungal carbon metabolism. Eukaryot Cell 9:1809–1815 [View Article][PubMed]
    [Google Scholar]
  49. Suzuki O. ( 1991). Recent trends of oleochemicals by biotechnology. Proceedings of World Conference on Oleochemicals into the 21st Century221–230 Applewhite T. H. F. Champaign, IL: American Oil Chemists’ Society;
    [Google Scholar]
  50. Tatusov R. L., Fedorova N. D., Jackson J. D., Jacobs A. R., Kiryutin B., Koonin E. V., Krylov D. M., Mazumder R., Mekhedov S. L. & other authors ( 2003). The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41 [View Article][PubMed]
    [Google Scholar]
  51. Vauterin M., Frankard V., Jacobs M. ( 1999). The Arabidopsis thaliana dhdps gene encoding dihydrodipicolinate synthase, key enzyme of lysine biosynthesis, is expressed in a cell-specific manner. Plant Mol Biol 39:695–708 [View Article][PubMed]
    [Google Scholar]
  52. Vicente G., Bautista L. F., Gutierrez F. J., Rodriguez R., Martinez V., Rodriguez-Frometa R. A., Ruiz-Vazquez R. M., Torres-Martinez S., Garre V. ( 2010). Direct transformation of fungal biomass from submerged cultures into biodiesel. Energy Fuels 24:3173–3178 [View Article]
    [Google Scholar]
  53. Waché Y., Aguedo M., Nicaud J. M., Belin J. M. ( 2003). Catabolism of hydroxyacids and biotechnological production of lactones by Yarrowia lipolytica. . Appl Microbiol Biotechnol 61:393–404[PubMed] [CrossRef]
    [Google Scholar]
  54. Wysocki S. J., Hähnel R. ( 1986). 3-Hydroxy-3-methylglutaryl-coenzyme A lyase deficiency: a review. J Inherit Metab Dis 9:225–233 [View Article][PubMed]
    [Google Scholar]
  55. Xu H., Andi B., Qian J., West A. H., Cook P. F. ( 2006). The α-aminoadipate pathway for lysine biosynthesis in fungi. Cell Biochem Biophys 46:43–64 [View Article][PubMed]
    [Google Scholar]
  56. Zhang Y., Adams I. P., 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 [View Article][PubMed]
    [Google Scholar]
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