Proteomics analysis of high lipid-producing strain Mucor circinelloides WJ11: An explanation for the mechanism of lipid accumulation at the proteomic level

Microbial Cell Factories

Volumn 15, Issue 1, 2016, Pages

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

^a JIANGNAN UNIVERSITY   (China)

^b SHANDONG UNIVERSITY OF TECHNOLOGY   (China)

^c Synergetic Innovation Center of Food Safety and Nutrition   (China)

^d UNIVERSITY OF HULL   (United Kingdom)

Author keywords

Lipid accumulation; Mucor circinelloides; Nitrogen deficiency; Proteomics

Indexed keywords

AMINO ACID; CARBON; LIPID; NITROGEN; PROTEOME;

BIOSYNTHESIS; CYTOLOGY; DRUG EFFECTS; FUNGAL GENE; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; MUCOR; PROCEDURES; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION;

AMINO ACIDS; CARBON; GENES, FUNGAL; LIPID METABOLISM; LIPIDS; METABOLIC NETWORKS AND PATHWAYS; MUCOR; NITROGEN; PROTEOME; PROTEOMICS; REAL-TIME POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRANSCRIPTION, GENETIC;

EID: 84957628656     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-016-0428-4     Document Type: Article

References (52)

1. Thorpe R, Ratledge C. Fatty acid distribution in triglycerides of yeasts grown on glucose or n-alkanes. J Gen Microbiol. 1972;72:151-63.
2. Ratledge C. The role of malic enzyme as the provider of NADPH in oleaginous microorganisms: a reappraisal and unsolved problems. Biotech Lett. 2014;36:1557-68.
3. Ratledge C, Wynn JP. The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol. 2002;51:1-51.
4. Ratledge C. Microbial production of gamma-linolenic acid. In: Akoh CC, editor. Handbook of functional lipids. Boca Raton: CRC Press; 2005. p. 19-45.
5. Botham PA, Ratledge C. A biochemical explanation for lipid accumulation in Candida 107 and other oleaginous micro-organisms. J Gen Microbiol. 1979;114:361-75.
6. Tang X, Chen H, Chen YQ, Chen W, Garre V, Song Y, Ratledge C. Comparison of biochemical activities between high and low lipid-producing strains of Mucor circinelloides: an explanation for the high oleaginicity of strain WJ11. PLoS ONE. 2015;10:e0128396.
7. Boulton CA, Ratledge C. Correlation of lipid accumulation in yeasts with possession of ATP: citrate lyase. J Gen Microbiol. 1981;127:169-76.
8. Tamano K, Bruno KS, Karagiosis SA, Culley DE, Deng S, Collett JR, Umemura M, Koike H, Baker SE, Machida M. Increased production of fatty acids and triglycerides in Aspergillus oryzae by enhancing expressions of fatty acid synthesis-related genes. Appl Microbiol Biotechnol. 2013;97:269-81.
9. Zhang H, Zhang L, Chen H, Chen YQ, Chen W, Song Y, Ratledge C. Enhanced lipid accumulation in the yeast Yarrowia lipolytica by over-expression of ATP: citrate lyase from Mus musculus. J Biotechnol. 2014;192:78-84.
10. Wynn JP, bin Abdul Hamid A, Ratledge C. The role of malic enzyme in the regulation of lipid accumulation in filamentous fungi. Microbiology. 1999;145:1911-7.
11. Wynn JP, Ratledge C. Malic enzyme is a major source of NADPH for lipid accumulation by Aspergillus nidulans. Microbiology. 1997;143:253-7.
12. Zhu Z, Zhang S, Liu H, Shen H, Lin X, Yang F, Zhou YJ, Jin G, Ye M, Zou H. A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat Commun. 2012;3:1112.
13. Liu Z, Gao Y, Chen J, Imanaka T, Bao J, Hua Q. Analysis of metabolic fluxes for better understanding of mechanisms related to lipid accumulation in oleaginous yeast Trichosporon cutaneum. Bioresour Technol. 2013;130:144-51.
14. Paula Alonso A, Dale VL, Shachar Hill Y. Understanding fatty acid synthesis in developing maize embryos using metabolic flux analysis. Metab Eng. 2010;12:488-97.
15. 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 Chlorella protothecoides. Plant Physiol. 2010;154:1001-11.
16. 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.
17. Zhao L, Zhang H, Wang L, Chen H, Chen YQ, Chen W, Song Y. 13 C-metabolic flux analysis of lipid accumulation in the oleaginous fungus Mucor circinelloides. Bioresour Technol. 2015;197:23-9.
18. Yang ZK, Ma YH, Zheng JW, Yang WD, Liu JS, Li HY. Proteomics to reveal metabolic network shifts towards lipid accumulation following nitrogen deprivation in the diatom Phaeodactylum tricornutum. J Appl Phycol. 2014;26:73-82.
19. Garnier M, Carrier G, Rogniaux H, Nicolau E, Bougaran G, Saint-Jean B, Cadoret J-P. Comparative proteomics reveals proteins impacted by nitrogen deprivation in wild-type and high lipid-accumulating mutant strains of Tisochrysis lutea. J Proteomics. 2014;105:107-20.
20. Song P, Li L, Liu J. Proteomic analysis in nitrogen-deprived Isochrysis galbana during lipid accumulation. PLoS ONE. 2013;8:e82188.
21. Liu H, Zhao X, Wang F, Li Y, Jiang X, Ye M, Zhao ZK, Zou H. Comparative proteomic analysis of Rhodosporidium toruloides during lipid accumulation. Yeast. 2009;26:553-66.
22. Chen H, Hao G, Wang L, Wang H, Gu Z, Liu L, Zhang H, Chen W, Chen YQ. Identification of a critical determinant that enables efficient fatty acid synthesis in oleaginous fungi. Sci Rep. 2015;5:11247.
23. Xia C, Zhang J, Zhang W, Hu B. A new cultivation method for microbial oil production: cell pelletization and lipid accumulation by Mucor circinelloides. Biotechnol Biofuels. 2011;4:1-10.
24. 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 γ-linolenic acid yield in Mucor circinelloides. Curr Microbiol. 2014;69:899-908.
25. Stacey G, Van Baalen C, Tabita FR. Nitrogen and ammonia assimilation in the cyanobacteria: regulation of glutamine synthetase. Arch Biochem Biophys. 1979;194:457-67.
26. Magasanik B, Kaiser CA. Nitrogen regulation in Saccharomyces cerevisiae. Gene. 2002;290:1-18.
27. Chipman D, Ze Barak, Schloss JV. Biosynthesis of 2-aceto-2-hydroxy acids: acetolactate synthases and acetohydroxyacid synthases. BBA Protein Struct Mol Enzymol. 1998;1385:401-19.
28. Myers JW. Dihydroxy acid dehydrase: an enzyme involved in the biosynthesis of isoleucine and valine. J Biol Chem. 1961;236:1414-8.
29. Chunduru SK, Mrachko GT, Calvo K. Mechanism of ketol acid reductoisomerase. Steady-state analysis and metal ion requirement. Biochemistry. 1989;28:486-93.
30. Ichihara A, Koyama E. Transaminase of branched chain amino acids. J Biochem. 1966;59:160-9.
31. Huber TA, Streeter JG. Asparagine biosynthesis in soybean nodules. Plant Physiol. 1984;74:605-10.
32. Fujioka M, Nakatani Y. Saccharopine dehydrogenase. Eur J Biochem. 1972;25:301-7.
33. Miyazaki J, Kobashi N, Nishiyama M, Yamane H. Characterization of homoisocitrate dehydrogenase involved in lysine biosynthesis of an extremely thermophilic bacterium, Thermus thermophilus HB27, and evolutionary implication of β-decarboxylating dehydrogenase. J Biol Chem. 2003;278:1864-71.
34. Kikuchi G. The glycine cleavage system: composition, reaction mechanism, and physiological significance. Mol Cell Biochem. 1973;1:169-87.
35. Lu SC. S-adenosylmethionine. Int J Biochem cell B. 2000;32:391-5.
36. Shin R, Berg RH, Schachtman DP. Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol. 2005;46:1350-7.
37. Guy C, Carter J. Effect of low temperature on the glutathione status of plant cells. Plant Cold Hardiness Freez Stress. 1982;2:169-79.
38. Kendrick A, Ratledge C. Desaturation of polyunsaturated fatty acids in Mucor circinelloides and the involvement of a novel membrane-bound malic enzyme. Eur J Biochem. 1992;209:667-73.
39. Marsh JJ, Lebherz HG. Fructose-bisphosphate aldolases: an evolutionary history. Trends Biochem Sci. 1992;17:110-3.
40. Song Y, Wynn JP, Li Y, Grantham D, Ratledge C. A pre-genetic study of the isoforms of malic enzyme associated with lipid accumulation in Mucor circinelloides. Microbiology. 2001;147:1507-15.
41. Zhang Y, Adams IP, Ratledge C. 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. 2007;153:2013-25.
42. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH. Glutathione in plants: an integrated overview. Plant, Cell Environ. 2012;35:454-84.
43. Machado C, Oliveira RCL, Boiteux S, Praekelt UM, Meacock PA, Menck CFM. Thi1, a thiamine biosynthetic gene in Arabidopsis thaliana, complements bacterial defects in DNA repair. Plant Mol Biol. 1996;31:585-93.
44. Machado CR, Praekelt UM, Oliveira RCL, Barbosa ACC, Byrne KL, Meacock PA, Menck CF. Dual role for the yeast THI4 gene in thiamine biosynthesis and DNA damage tolerance. J Mol Biol. 1997;273:114-21.
45. Wynn JP, Hamid AA, Li Y, Ratledge C. Biochemical events leading to the diversion of carbon into storage lipids in the oleaginous fungi Mucor circinelloides and Mortierella alpina. Microbiology. 2001;147:2857-64.
46. Hermeking H, Benzinger A. 14-3-3 proteins in cell cycle regulation. Semin Cancer Biol. 2006;16:183-92.
47. Choi YE, Kwon KW, Lee JC, Woo SY. Expression of the rice cytoplasmic cysteine synthase gene in tobacco reduces ozone-induced damage. Plant Biotechnol Rep. 2007;1:93-100.
48. Bell A, Monaghan P, Page AP. Peptidyl-prolyl cis-trans isomerases (immunophilins) and their roles in parasite biochemistry, host-parasite interaction and antiparasitic drug action. Int J Parasitol. 2006;36:261-76.
49. Tang X, Zhao L, Chen H, Chen YQ, Chen W, Song Y, Ratledge C. 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. 2015;10:e0137543.
50. Chaney AL, Marbach EP. Modified reagents for determination of urea and ammonia. Clin Chem. 1962;8:130-2.
51. Liu X, Wu H, Ji C, Wei L, Zhao J, Yu J. An integrated proteomic and metabolomic study on the chronic effects of mercury in Suaeda salsa under an environmentally relevant salinity. PLoS ONE. 2013;8:e64041.
52. Chen Y, Pang Q, Dai S, Wang Y, Chen S, Yan X. Proteomic identification of differentially expressed proteins in Arabidopsis in response to methyl jasmonate. J Plant Physiol. 2011;168:995-1008.