Proteome analysis of Aspergillus niger: Lactate added in starch-containing medium can increase production of the mycotoxin fumonisin B2by modifying acetyl-CoA metabolism

BMC Microbiology

Volumn 9, Issue , 2009, Pages

  Sørensen, Louise M ^a,b   Lametsch, Rene ^b   Andersen, Mikael R ^a   Nielsen, Per V ^c   Frisvad, Jens C ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c IPU Denmark   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; AMMONIA; AMYLASE; AURASPERONE B; DESMETHYLKOTANIN; FATTY ACID SYNTHASE; FUMONISIN B2; GLUCOSE 6 PHOSPHATE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE (NADP); HEAT SHOCK PROTEIN; ISOCITRATE DEHYDROGENASE; KOTANIN; LACTIC ACID; MALFORMIN A; MALFORMIN C; OCHRATOXIN; OCHRATOXIN ALPHA; ORLANDIN; PENTOSE PHOSPHATE; PYRANONIGRIN A; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; STARCH; TENSIDOL B; TRICARBOXYLIC ACID; UNCLASSIFIED DRUG; FUMONISIN; MYCOTOXIN; PROTEOME;

ALPHA CHAIN; AMINO ACID SEQUENCE; ARTICLE; ASPERGILLUS NIGER; CITRIC ACID CYCLE; CLUSTER ANALYSIS; CULTURE MEDIUM; ENZYME METABOLISM; FATTY ACID SYNTHESIS; FUNGAL STRAIN; FUNGUS GROWTH; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPOTHESIS; IMAGE ANALYSIS; INCUBATION TIME; INOCULATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METABOLITE; NONHUMAN; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEOMICS; REGULATORY MECHANISM; FUNGUS SPORE; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; PRINCIPAL COMPONENT ANALYSIS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ASPERGILLUS NIGER; FUNGI;

ACETYL COENZYME A; ASPERGILLUS NIGER; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLUSTER ANALYSIS; CULTURE MEDIA; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FUMONISINS; LACTIC ACID; MYCOTOXINS; PRINCIPAL COMPONENT ANALYSIS; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPORES, FUNGAL; STARCH; TANDEM MASS SPECTROMETRY;

EID: 77449094201     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-9-255     Document Type: Article

References (78)

1. JI Pitt AD Hocking, Fungi and food spoilage London, U.K.: Blackie Academic and Professional 1997
2. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. RP de Vries J Visser, Microbiol Mol Biol Rev 2001 65 497 522 10.1128/MMBR.65.4.497-522.2001 11729262 (Pubitemid 33123516)
3. On the safety of Aspergillus niger - a review. E Shuster N Dunn-Coleman JC Frisvad PWM van Dijck, Appl Microbiol Biotechnol 2002 59 426 435 10.1007/s00253-002-1032-6 12172605 (Pubitemid 35002176)
4. Physiology and biotechnology of Aspergillus. OP Ward WM Qin J Dhanjoon J Ye A Singh, Adv Appl Microbiol 2006 58 1 75 full-text 16509442
5. Ochratoxin A production by strains of Aspergillus niger var. niger. ML Abarca MR Bragulat G Castell FJ Cabães, Appl Environ Microbiol 1994 60 2650 2652 8074536 (Pubitemid 24205774)
6. Fumonisin B2 production by Aspergillus niger. JC Frisvad J Smedsgaard RA Samson TO Larsen U Thrane, J Agric Food Chem 2007 55 9727 9732 10.1021/jf0718906 17929891
7. Secondary metabolism: Regulation and role in fungal biology. EM Fox BJ Howlett, Curr Opin Microbiol 2008 11 6 481 7 10.1016/j.mib.2008.10.007 18973828
8. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. O Bayram S Krappmann M Ni JW Bok K Helmstaedt O Valerius S Braus-Stromeyer NJ Kwon NP Keller JH Yu GH Braus, Science 2008 320 1504 1506 10.1126/science.1155888 18556559 (Pubitemid 351929431)
9. Relationship between secondary metabolism and fungal development. AM Calvo RA Wilson JW Bok NP Keller, Microbiol Mol Biol Rev 2002 66 447 459 10.1128/MMBR.66.3.447-459.2002 12208999
10. Specific association of fungi to foods and influence of physical environmental factors. O Filtenborg JC Frisvad RA Samson, Introduction to food- and airborne fungi Utrecht: Centraalbureau voor Schimmelcultures, Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O, 6 2002 306 320
11. Polyphasic taxonomy of Penicillium. A guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. JC Frisvad RA Samson, Studies in Mycology 2004 49 1 173
12. Regulation of fumonisin biosynthesis in Fusarium verticillioides -maize system. US Sagaram M Kolomiets W Shim, Plant Path J 2006 22 203 210
13. Biosynthesis of sphinganine-analog mycotoxins. L Du X Zhu R Gerber J Huffman L Lou J Jorgenson F Yu K Zaleta-Rivera Q Wang, J Ind Microbiol Biotechnol 2008 35 455 464 10.1007/s10295-008-0316-y 18214562
14. Cytotoxicity assays for mycotoxins produced by Fusarium strains: a review. AC Gutleb E Morrison AJ Murk, Environ Tox Pharmcol 2002 11 309 320 10.1016/S1382-6689(02)00020-0 (Pubitemid 34694011)
15. Structure-activity-relationships of fumonisins in short-term carcinogenesis and cytotoxicity assays. WCA Gelderblom ME Cawood SD Snyman R Vleggaar WFO Marasas, Food Chem Toxicol 1993 31 407 414 10.1016/0278-6915(93) 90155-R 8514212 (Pubitemid 23181256)
16. Simultaneous occurrence of fumonisin B-1 and other mycotoxins in moldy corn collected from the Peoples-Republic-Of-China in regions with high incidences of esophageal cancer. FS Chu GY Li, Appl Environ Microbiol 1994 60 847 852 8161178
17. Fusarium moniliforme contamination of maize in esophageal cancer areas in Transkei. WFO Marasas K Jaskiewicz FS Venter DJ Van Schalkwyk, S Afr Med J 1988 74 110 114 3399988
18. Natural occurrence of some Fusarium mycotoxins in corn from low and high esophageal cancer prevalence areas of the Transkei, Southern Africa. EW Sydenham PG Thiel WFO Marasas GS Shephard DJ Van Schalkwyk KR Koch, J Agric Food Chem 1990 38 1900 1903 10.1021/jf00100a004
19. Fumonisin occurrence in corn from high-risk and low-risk areas for human esophageal cancer in China. T Yoshizawa A Yamashita Y Luo, Appl Environ Microbiol 1994 60 1626 1629 8017941 (Pubitemid 24144824)
20. Fumonisins - novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. WCA Gelderblom K Jaskiewicz WFO Marasas PG Thiel RM Horak R Vleggaar NPJ Kriek, Appl Environ Microbiol 1988 54 1806 1811 2901247
21. Aspergillus niger genomics: Past, present and into the future. SE Baker, Med Mycol 2006 44 17 S21 10.1080/13693780600921037 17050415
22. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. HJ Pel JH de Winde DB Archer PS Dyer G Hofmann PJ Schaap G Turner RP de Vries R Albang K Albermann MR Andersen JD Bendtsen JAE Benen M van den Berg S Breestraat MX Caddick R Contreras M Cornell PM Coutinho EGJ Danchin AJM Debets P Dekker PWM van Dijck A van Dijk L Dijkhuizen AJM Driessen C d'Enfert S Geysens C Goosen GSP Groot PWJ De Groot T Guillemette B Henrissat M Herweijer JPTW van den Hombergh CAMJ van den Hondel RTJM van der Heijden RM van der Kaaij FM Klis HJ Kools CP Kubicek PA van Kuyk J Lauber X Lu MJEC van der Maarel R Meulenberg H Menke MA Mortimer J Nielsen SG Oliver M Olsthoorn K Pal NNME van Peij AFJ Ram U Rinas JA Roubos CMJ Sagt M Schmoll JB Sun D Ussery J Varga W Vervecken PJJ van de Vondervoort H Wedler HAB Wosten AP Zeng AJJ van Ooyen J Visser H Stam, Nat Biotechnol 2007 25 221 231 10.1038/nbt1282 17259976 (Pubitemid 46227122)
23. Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. RH Proctor DW Brown RD Plattner AE Desjardins, Fungal Genet Biol 2003 38 237 249 10.1016/S1087-1845(02)00525-X 12620260
24. Fumonisin B2 production by Aspergillus niger in Thai coffee beans. P Noonim W Mahakarnchanakul KF Nielsen JC Frisvad RA Samson, Food Addit Contam 2009 26 94 100 10.1080/02652030802366090
25. Proteomic studies in biomedically and industrially relevant fungi. S Carberry S Doyle, Cytotechnology 2007 53 95 100 10.1007/s10616-007-9054-7 19003194 (Pubitemid 46944874)
26. Proteomics of filamentous fungi. Y Kim MP Nandakumar MR Marten, Trends Biotechnol 2007 25 395 400 10.1016/j.tibtech.2007.07.008 17681627 (Pubitemid 350147110)
27. The state of proteome profiling in the fungal genus Aspergillus. Y Kim MP Nandakumar MR Marten, Brief Func Genom Proteom 2008 7 87 94 10.1093/bfgp/elm031 (Pubitemid 351728950)
28. Current status of systems biology in Aspergilli. MR Andersen J Nielsen, Fungal Genet Biol 2009 46 180 S190 10.1016/j.fgb.2008.07.006 18684401
29. Micro-scale extraction procedure for standardized screening of fungal metabolite production in cultures. J Smedsgaard, J Chromatogr A 1997 760 264 270 10.1016/S0021-9673(96)00803-5 9062989 (Pubitemid 27085582)
30. Regio- and stereoselective intermolecular oxidative phenol coupling in kotanin biosynthesis by Aspergillus niger. W Hüttel M Müller, Chembiochem 2007 8 521 529 10.1002/cbic.200600434 17315249 (Pubitemid 47183648)
31. Saccharomyces cerevisiae JEN1 promoter activity is inversely related to concentration of repressing sugar. P Chambers A Issaka SP Palecek, Appl Environ Microbiol 2004 70 8 17 10.1128/AEM.70.1.8-17.2004 14711620 (Pubitemid 38090182)
32. Polyol synthesis in Aspergillus niger : Influence of oxygen availability, carbon and nitrogen sources on the metabolism. A Diano S Bekker-Jensen J Dynesen J Nielsen, Biotechnol Bioeng 2006 94 899 908 10.1002/bit.20915 16718677 (Pubitemid 44186897)
33. Effective lead selection for improved protein production in Aspergillus niger based on integrated genomics. DI Jacobs MM Olsthoorn I Maillet M Akeroyd S Breestraat S Donkers RA van der Hoeven CA van den Hondel R Kooistra T Lapointe H Menke R Meulenberg M Misset WH Müller NN van Peij A Ram S Rodriguez MS Roelofs JA Roubos MW van Tilborg AJ Verkleij HJ Pel H Stam CM Sagt, Fungal Genet Biol 2009 46 141 S152 10.1016/j.fgb.2008.08.012 18824119
34. Proteome map of Aspergillus nidulans during osmoadaptation. Y Kim MP Nandakumar MR Marten, Fungal Genet Biol 2007 44 886 895 10.1016/j.fgb.2006.12. 001 17258477 (Pubitemid 47176937)
35. Transcriptomic comparison of Aspergillus niger growing on two different sugars reveals coordinated regulation of the secretory pathway. TR Jørgensen T Goosen CA Hondel AF Ram JJ Iversen, BMC Genomics 2009 10 44 10.1186/1471-2164-10-44 19166577
36. Robust multi-scale clustering of large DNA microarray datasets with the consensus algorithm. T Grotkjær O Winther B Regenberg J Nielsen LK Hansen, Bioinformatics 2006 22 58 67 10.1093/bioinformatics/bti746 16257984 (Pubitemid 43057009)
37. Swiss Institute of Bioinformatics. http://www.expasy.ch/sprot/
38. National Center for Biotechnology Information. http://www.ncbi.nlm.nih. gov/
39. Protein knowledgebase UniProtKB. http://www.uniprot.org/
40. Basic local alignment search tool. SF Altschul W Gish W Miller EW Myers DJ Lipman, J Mol Biol 1990 215 403 410 2231712 (Pubitemid 20364473)
41. European Bioinformatics Institute. http://www.ebi.ac.uk/
42. Participation in aflatoxin biosynthesis by a reductase enzyme encoded by vrdA gene outside the aflatoxin gene cluster. Y Shima M Shiina T Shinozawa Y Ito H Nakajima Y Adachi K Yabe, Fungal Genet Biol 2009 46 221 231 10.1016/j.fgb.2008.12.005 19211038
43. The ALD6 gene product is indispensable for providing NADPH in yeast cells lacking glucose-6-phosphate dehydrogenase activity. D Grabowska A Chelstowska, J Biol Chem 2003 278 13984 13988 10.1074/jbc.M210076200 12584194 (Pubitemid 36799941)
44. Regulation of the pentose phosphate pathway in the fungus Aspergillus nidulans. The effect of growth with nitrate. O Hankinson DJ Cove, J Biol Chem 1974 249 2344 2353 4274591
45. Sources of NADPH and expression of mammalian NADP+-specific isocitrate dehydrogenases in Saccharomyces cerevisiae. KI Minard GT Jennings TM Loftus D Xuan L McAlister-Henn, J Biol Chem 1998 273 31486 31493 10.1074/jbc.273.47.31486 9813062 (Pubitemid 28533170)
46. Increased NADPH concentration obtained by metabolic engineering of the pentose phosphate pathway in Aspergillus niger. BR Poulsen J Nohr S Douthwaite LV Hansen JJL Iversen J Visser GJG Ruijter, Febs Journal 2005 272 1313 1325 10.1111/j.1742-4658.2005.04554.x 15752350 (Pubitemid 40444923)
47. Re-characterisation of Saccharomyces cerevisiae Ach1p: Fungal CoA-transferases are involved in acetic acid detoxification. CB Fleck M Brock, Fungal Genet Biol 2009 46 473 485 10.1016/j.fgb.2009.03.004 19298859
48. Functional characterization and localization of acetyl-CoA hydrolase, Ach1p, in Saccharomyces cerevisiae. LM Buu YC Chen FJS Lee, J Biol Chem 2003 278 17203 17209 10.1074/jbc.M213268200 12606555 (Pubitemid 36799601)
49. Role of acetyl coenzyme A synthesis and breakdown in alternative carbon source utilization in Candida albicans. AJ Carman S Vylkova MC Lorenz, Eukaryotic Cell 2008 7 1733 1741 10.1128/EC.00253-08 18689527
50. Purification and characterization of glucose-6-phosphate-dehydrogenase from Aspergillus niger and Aspergillus nidulans. LMJ Wennekes T Goosen PJM Van den Broek HWJ Van den Broek, J Gen Microbiol 1993 139 2793 2800 8277259 (Pubitemid 2009051)
51. Oxidative stress-activated zinc cluster protein Stb5 has dual activator/repressor functions required for pentose phosphate pathway regulation and NADPH production. M Larochelle S Drouin F Robert B Turcotte, Mol Cell Biol 2006 26 6690 6701 10.1128/MCB.02450-05 16914749 (Pubitemid 44277903)
52. Oxidative stress-associated impairment of glucose and ammonia metabolism in the filamentous fungus Aspergillus niger B1-D. Q Li R Abrashev LM Harvey B McNeil, Mycological Research 2008 112 1049 1055 10.1016/j.mycres.2008.03.004 18693104
53. Regulation of secondary metabolism in filamentous fungi. J Yu N Keller, Ann Rev Phytopath 2005 43 437 458 10.1146/annurev.phyto.43.040204.140214 (Pubitemid 41318879)
54. Acetyl coenzyme A stimulates RNA polymerase II transcription and promoter binding by transcription factor IID in the absence of histones. SK Galasinski TN Lively AG de Barron JA Goodrich, Mol Cell Biol 2000 20 1923 1930 10.1128/MCB.20.6.1923-1930.2000 10688640
55. Inhibition of acetyl coenzyme a carboxylase activity restores expression of the INO1 gene in a snf1 mutant strain of Saccharomyces cerevisiae. MK Shirra J Patton-Vogt A Ulrich O Liuta-Tehlivets SD Kohlwein SA Henry KM Arndt, Mol Cell Biol 2001 21 5710 5722 10.1128/MCB.21.17.5710-5722.2001 11486011 (Pubitemid 32737790)
56. Phosphatidylinositol biosynthesis: Biochemistry and regulation. ME Gardocki N Jani JM Lopes, Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids 2005 1735 89 100 10.1016/j.bbalip.2005.05.006 (Pubitemid 40961965)
57. Glycosylinositolphosphoceramides in Aspergillus fumigatus. C Simenel B Coddeville M Delepierre JP Latge T Fontaine, Glycobiology 2008 18 84 96 10.1093/glycob/cwm122 17971386
58. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. S Spange T Wagner T Heinzel OH Kramer, Int J Biochem Cell Biol 2009 41 185 198 10.1016/j.biocel.2008.08.027 18804549
59. The initiation and pattern of spread of histones H4 acetylation parallel the order of transcriptional activation of genes in the aflatoxin cluster. LV Roze AE Arthur S Hong A Chanda JE Linz, Mol Microbiol 2007 66 713 726 10.1111/j.1365-2958.2007.05952.x 17919289 (Pubitemid 47621858)
60. Histone deacetylase activity regulates chemical diversity in Aspergillus. EK Shwab JW Bok M Tribus J Galehr S Graessle N Keller, Eukaryotic Cell 2007 6 1656 1664 10.1128/EC.00186-07 17616629 (Pubitemid 47483608)
61. Role of AREA, a regulator of nitrogen metabolism, during colonization of maize kernels and fumonisin biosynthesis in Fusarium verticillioides. H Kim CP Woloshuk, Fungal Genet Biol 2008 45 947 953 10.1016/j.fgb.2008.03.007 18440841
62. Amylopectin induces fumonisin B-1 production by Fusarium verticillioides during colonization of maize kernels. BH Bluhm CP Woloshuk, Mol Plant Microbe Interact 2005 18 1333 1339 10.1094/MPMI-18-1333 16478053
63. The antifungal effect of fumonisin B-1 on Fusarium and other fungal species. Z Keyser HF Vismer JA Klaasen PW Snijman WFO Marasas, S Afr J Sci 1999 95 455 458 (Pubitemid 30018426)
64. Optimisation of a 2-D gel electrophoresis protocol for the human-pathogenic fungus Aspergillus fumigatus. O Kniemeyer F Lessing O Scheibner C Hertweck AA Brakhage, Curr Genet 2006 49 178 189 10.1007/s00294-005-0047-9 16362819 (Pubitemid 43300242)
65. Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. A Shevchenko M Wilm O Vorm M Mann, Anal Chem 1996 68 850 858 10.1021/ac950914h 8779443 (Pubitemid 26101214)
66. Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J Gobom E Nordhoff E Mirgorodskaya R Ekman P Roepstorff, J Mass Spectrom 1999 34 105 116 10.1002/(SICI)1096-9888(199902)34:2<105::AID-JMS7683.0.CO;2-4 10093212 (Pubitemid 129500440)
67. Matrix Science. http://www.matrixscience.com/
68. Metabolic model integration of the bibliome, genome, metabolome and reactome of Aspergillus niger. MR Andersen ML Nielsen J Nielsen, Mol Sys Biol 2008 4 178 18364712 (Pubitemid 351441042)
69. Fungal metabolite screening: database of 474 mycotoxins and fungal metabolites for dereplication by standardised liquid chromatography-UV-mass spectrometry methodology. KF Nielsen J Smedsgaard, J Chromatogr A 2003 1002 111 136 10.1016/S0021-9673(03)00490-4 12885084 (Pubitemid 36700450)
70. Degradation of ochratoxin A by Aspergillus species. J Varga K Rigá J Téren, Int J Food Microbiol 2000 59 1 7 10.1016/S0168-1605(00)00230-0 10946833 (Pubitemid 30408282)
71. Structure of malformin A, a phytotoxic metabolite produced by Aspergillus niger. K Kim F Sugawara S Yoshida N Murofushi N Takahashi RW Curtis, Biosci Biotechnol Biochem 1993 57 240 243 10.1271/bbb.57.240
72. Production and antibacterial activity of malformin C, a toxic metabolite of Aspergillus niger. B Kobbe M Cushman GN Wogan AL Demain, Appl Environ Microbiol 1977 33 996 997 869543 (Pubitemid 8087967)
73. Orlandin: A nontoxic fungal metabolite with plant growth inhibiting properties. HG Cutler FG Crumley RH Cox O Hernandez RJ Cole JW Dorner, J Agric Food Chem 1979 27 592 595 10.1021/jf60223a043 447931
74. New dimeric naphthopyrones from Aspergillus niger. K Akiyama S Teraguchi Y Hamasaki M Mori K Tatsumi K Ohnishi H Hayashi, J Nat Prod 2003 66 136 139 10.1021/np020174p 12542363 (Pubitemid 36150835)
75. New naphthopyrones from Aspergillus fonsecaeus. HA Priestap, Tetrahendon 1984 40 3617 3624 10.1016/S0040-4020(01)88792-5
76. New natural products from the sponge-derived fungus Aspergillus niger. J Hiort K Maksimenka M Reichert S Perovic-Ottstadt WH Lin V Wray K Steube K Schaumann H Weber P Proksch R Ebel WEG Muiller G Bringmann, J Nat Prod 2004 67 1532 1543 10.1021/np030551d 15387655 (Pubitemid 39298623)
77. Reassessing the structure of pyranonigrin. G Schlingmann T Taniguchi H He R Bigelis HY Yang FE Koehn GT Carter N Berova, J Nat Prod 2007 70 1180 1187 10.1021/np070175n 17604395 (Pubitemid 47279912)
78. Tensidols, new potentiators of antifungal miconazole activity, produced by Aspergillus niger FKI-2342. T Fukuda Y Hasegawa K Hagimori Y Yamaguchi R Masuma H Tomoda S mura, J Antibiot 2006 59 480 485 10.1038/ja.2006.67 17080684 (Pubitemid 44520166)