Complete genome sequence of a high lipid-producing strain of mucor circinelloides WJ11 and comparative genome analysis with a low lipid-producing strain CBS 277.49

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Tang, Xin ^a   Zhao, Lina ^a   Chen, Haiqin ^a,b   Chen, Yong Q ^a,b   Chen, Wei ^a,b   Song, Yuanda ^a   Ratledge, Colin ^c  

^a JIANGNAN UNIVERSITY   (China)

^b Synergistic Innovation Center for Food Safety and Nutrition   (China)

^c UNIVERSITY OF HULL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; FUNGAL DNA; GENOMIC DNA; LIPID;

ARTICLE; CARBON METABOLISM; CONTROLLED STUDY; DNA CONTENT; FUNGAL GENE; FUNGAL GENOME; FUNGAL STRAIN; GENE SEQUENCE; GENOME ANALYSIS; GENOME SIZE; LIPID METABOLISM; LIPID STORAGE; MUCOR CIRCINELLOIDES; NONHUMAN; STRAIN DIFFERENCE; CHROMOSOMAL MAPPING; DNA SEQUENCE; GENETICS; GENOMICS; MUCOR;

CHROMOSOME MAPPING; GENOME, FUNGAL; GENOMICS; LIPID METABOLISM; MUCOR; SEQUENCE ANALYSIS, DNA;

EID: 84944732514     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137543     Document Type: Article

References (49)

1. Ratledge C. The role of malic enzyme as the provider of NADPH in oleaginous microorganisms: a reappraisal and unsolved problems. Biotechnol Lett. 2014: 36, 1557-1568. doi: 10.1007/s10529-014-1532-3 PMID: 24752812
2. Liang M-H, Jiang J-G. Advancing oleaginous microorganisms to produce lipid via metabolic engineering technology. Prog Lipid Res. 2013; 52: 395-408. doi: 10.1016/j.plipres.2013.05.002 PMID: 23685199
3. Wanasundara UN, Wanasundara JPD. Gamma-linolenic acid: purification and functionality. In: Akoh CC, editor. Handbook of functional lipids. CRC press; 2005. pp. 47-75.
4. Wynn JP, bin Abdul Hamid A, Ratledge C. The role of malic enzyme in the regulation of lipid accumulation in filamentous fungi. Microbiology. 1999; 145:1911-1917. PMID: 10463157
5. Wynn JP, Hamid AA, Li Y, Ratledge C. Biochemical events leading to the diversion of carbon into storage lipids in the oleaginous fungi Mucorcircinelloides and Mortierella alpina. Microbiology. 2001; 147: 2857-2864. PMID: 11577164
6. Rodríguez-Frómeta RA, Gutiérrez A, Torres-Martínez S, Garre V. Malic enzyme activity is not the only bottleneck for lipid accumulation in the oleaginous fungus Mucorcircinelloides. Appl Microbiol Biotechnol. 2013; 97: 3063-3072. doi: 10.1007/s00253-012-4432-2 PMID: 23053085
7. Ratledge C. Microbial production of gamma-linolenic acid. In: Akoh CC, editor. Handbook of functional lipids. CRC press; 2005. pp. 19-45.
8. Ratledge C, Wynn JP. The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol. 2002; 51:1-51. PMID: 12236054
9. Tang X, Zhang H, Chen H, Chen YQ, Chen W, Song Y. Effects of 20 standard amino acids on the growth, total fatty acids production, and y-linolenic acid yield in Mucorcircinelloides. Curr Microbiol. 2014; 69: 899-908. doi: 10.1007/s00284-014-0671-z PMID: 25117649
10. Zhang Y, Adams IP, Ratledge C. Malic enzyme: the controlling activity for lipid production? Overexpression of malic enzyme in Mucorcircinelloides leads to a 2.5-fold increase in lipid accumulation. Microbiology.2007; 153: 2013-2025. PMID: 17600047
11. Tang X, Chen H, Chen YQ, Chen W, Garre V, Song Y, et al. Comparison of biochemical activities between high and low lipid-producing strains of Mucorcircinelloides: an explanation forthe high oleaginicity of strain WJ11. PLoS One. 2015; 10: e0128396. doi: 10.1371/journal.pone.0128396 PMID: 26046932
12. Zhao G, Yao Y, Chen W, Cao X. Comparison and analysis of the genomes of two Aspergillus oryzae strains. J Agric Food Chem. 2013; 61: 7805-7809. doi: 10.1021/jf400080g PMID: 23889147
13. Kendrick A, Ratledge C. Desaturation of polyunsaturated fatty acids in Mucorcircinelloides and the involvement of a novel membrane-bound malic enzyme. Eur J Biochem. 1992; 209: 667-673. PMID: 1425673
14. Zhang HB, Zhao X, Ding X, Paterson AH, Wing RA. Preparation of megabase-size DNA from plant nuclei. Plant J. 1995; 7:175-184.
15. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008; 18: 821-829. doi: 10.1101/gr.074492.107 PMID: 18349386
16. Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, Hannick LI, et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 2003; 31: 5654-5666. PMID: 14500829
17. Stanke M, Diekhans M, Baertsch R, Haussler D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics. 2008; 24: 637-644. doi: 10.1093/bioinformatics/btn013 PMID: 18218656
18. Majoros WH, Pertea M, Salzberg SL. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics. 2004; 20: 2878-2879. PMID: 15145805
19. Lukashin AV, Borodovsky M. GeneMark. hmm: new solutions for gene finding. Nucleic Acids Res. 1998; 26:1107-1115. PMID: 9461475
20. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O'Donnell CJ, de Bakker PI. SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics. 2008; 24: 2938-2939. doi: 10.1093/bioinformatics/btn564 PMID: 18974171
21. Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 2008; 9: R7. doi: 10.1186/gb-2008-9-1-r7 PMID: 18190707
22. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, et al. InterProScan: protein domains identifier. Nucleic Acids Res. 2005; 33: W116-W120. PMID: 15980438
23. Delcher AL, Salzberg SL, Phillippy AM. Using MUMmerto identify similar regions in large sequence sets. Curr Protoc Bioinf. 2003:10.13.11-10.13.18.
24. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003; 13: 2178-2189. PMID: 12952885
25. Wang L, Chen W, Feng Y, Ren Y, Gu Z, Chen H, et al. Genome characterization of the oleaginous fungus Mortierella alpina. PloS one. 2011; 6: e28319. doi: 10.1371/journal.pone.0028319 PMID: 22174787
26. Arisan-Atac I, Wolschek MF, Kubicek CP. Trehalose-6-phosphate synthase A affects citrate accumulation by Aspergillus niger under conditions of high glycolytic flux. FEMS Microbiol Lett. 1996; 140: 77-83. PMID: 8666204
27. Botham PA, Ratledge C. A biochemical explanation for lipid accumulation in Candida 107 and other oleaginous micro-organisms. J Gen Microbiol. 1979; 114: 361-375. PMID: 44315
28. Wynn JP, Ratledge C. Malic enzyme is a major source of NADPH for lipid accumulation by Aspergillus nidulans. Microbiology. 1997; 143: 253-257.
29. Hao G, Chen H, Wang L, Gu Z, Song Y, Zhang H, et al. Role of malic enzyme during fatty acid synthesis in oleaginous fungus Mortierella alpina. Appl Environ Microbiol. 2014; 80: 2672-2678. doi: 10.1128/AEM.00140-14 PMID: 24532075
30. Li Z, Sun H, Mo X, Li X, Xu B, Tian P. Overexpression of malic enzyme (ME) of Mucor circinelloides improved lipid accumulation in engineered Rhodotorula glutinis. Appl Microbiol Biotechnol. 2013; 97: 4927-4936. doi: 10.1007/s00253-012-4571-5 PMID: 23179623
31. Vongsangnak W, Zhang Y, Chen W, Ratledge C, Song Y. Annotation and analysis of malic enzyme genes encoding for multiple isoforms in the fungus Mucor circinelloides CBS 277.49. Biotechnol Lett. 2012; 34: 941-947. doi: 10.1007/s10529-012-0859-x PMID: 22367279
32. Boulton CA, Ratledge C. Correlation of lipid accumulation in yeasts with possession of ATP: citrate lyase. J Gen Microbiol. 1981; 127:169-176.
33. Tamano K, Bruno KS, Karagiosis SA, Culley DE, Deng S, Collett JR, et al. Increased production of fatty acids and triglycerides in Aspergillus oryzae by enhancing expressions of fatty acid synthesis-related genes. Appl Microbiol Biotechnol. 2013; 97: 269-281. doi: 10.1007/s00253-012-4193-y PMID: 22733113
34. Zhang H, Zhang L, Chen H, Chen YQ, Chen W, Song Y, et al. Enhanced lipid accumulation in the yeast Yarrowia lipolytica by over-expression of ATP: citrate lyase from Mus musculus. J Biotechnol. 2014; 192: 78-84. PMID: 25450640
35. Csernetics Á, Nagy G, Iturriaga EA, Szekeres A, Eslava AP, Vágvölgyi C, et al. Expression of three isoprenoid biosynthesis genes and their effects on the carotenoid production of the zygomycete Mucor circinelloides. Fungal Genet Biol. 2011; 48: 696-703. doi: 10.1016/j.fgb.2011.03.006 PMID: 21443966
36. Navarro E, Ruiz-Pérez VL, Torres-Martínez S. Over expression of the crg A gene abolishes light requirement for carotenoid biosynthesis in Mucor circinelloides. Eur J Biochem. 2001; 267: 800-807.
37. Lim H, Choi HT. Enhanced expression of chitinase during the autolysis of mushroom in Coprinellus congregatus. J Microbiol. 2009; 47: 225-228. doi: 10.1007/s12275-008-0247-3 PMID: 19412609
38. Chen YL, Montedonico AE, Kauffman S, Dunlap JR, Menn FM, Reynolds TB. Phosphatidylserine synthase and phosphatidylserine decarboxylase are essential for cell wall integrity and virulence in Candida albicans. Mol Microbiol. 2010; 75:1112-1132. doi: 10.1111/j.1365-2958.2009.07018.x PMID: 20132453
39. Mumby MC, Walter G. Protein serine/threonine phosphatases: structure, regulation, and functions in cell growth. Physiol Rev. 1993; 73: 673-699. PMID: 8415923
40. 2+-ATPase, is involved in stress tolerance and virulence in Cryptococcus neoformans. Infect Immun. 2007; 75: 3394-3405. PMID: 17502401
41. PaulaAlonso A, Dale VL, Shachar-Hill Y. Understanding fatty acid synthesis in developing maize embryos using metabolic flux analysis. Metab Eng. 2010; 12: 488-497. doi: 10.1016/j.ymben.2010.04.002 PMID: 20406696
42. Xiong W, Liu L, Wu C, Yang C, Wu Q. 13C-tracer and gas chromatography-mass spectrometry analyses reveal metabolic flux distribution in the oleaginous microalga Chlorellaprotothecoides. Plant Physiol. 2010; 154:1001-1011. doi: 10.1104/pp.110.158956 PMID: 20720172
43. Wasylenko TM, Ahn WS, Stephanopoulos G. The oxidative pentose phosphate pathway is the primary source of NADPH for lipid overproduction from glucose in Yarrowia lipolytica. Metab Eng. 2015; 30: 27-39. doi: 10.1016/j.ymben.2015.02.007 PMID: 25747307
44. Vigeolas H, Waldeck P, Zank T, Geigenberger P. Increasing seed oil content in oil-seed rape (Brassica napus L.) by over-expression of a yeast glycerol-3-phosphate dehydrogenase under the control of a seed-specific promoter. Plant Physiol. 2007; 5: 431-441.
45. Yang W, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB. A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiol. 2012; 160: 638-652. doi: 10.1104/pp.112.201996 PMID: 22864585
46. Shi Y, Cheng D. Beyond triglyceride synthesis: the dynamic functional roles of MGAT and DGAT enzymes in energy metabolism. Am J Physiol-Endocrinol Metab. 2009; 297: E10-E18. doi: 10.1152/ajpendo.90949.2008 PMID: 19116371
47. Padham AK, Hopkins MT, Wang T-W, McNamara LM, Lo M, Richardson LG, et al. Characterization of a plastid triacylglycerol lipase from Arabidopsis. Plant physiol. 2007; 143:1372-1384. PMID: 17259290
48. Germain V, Rylott EL, Larson TR, Sherson SM, Bechtold N, Carde JP, et al. Requirement for 3-ketoa-cyl-CoA thiolase-2 in peroxisome development, fatty acid β-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant Physiol. 2001; 28:1-12.
49. Hosaka K, Mishina M, Tanaka T, Kamiryo T, Numa S. Acyl-Coenzyme - A Synthetase I from Candida lipolytica. Eur J Biochem. 1979; 93:197-203. PMID: 108099