The carbon starvation response of Aspergillus niger during submerged cultivation: Insights from the transcriptome and secretome

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Nitsche, Benjamin M ^a,b   Jørgensen, Thomas R ^a,c,d   Akeroyd, Michiel ^e   Meyer, Vera ^b,c   Ram, Arthur F J ^a,c  

^a LEIDEN UNIVERSITY   (Netherlands)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^c KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

^d NOVO NORDISK A S   (Denmark)

^e DSM BIOTECHNOLOGY CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHITINASE; FUNGAL PROTEIN; GLUCAN GLUCOSIDASE; HYDROLASE; PHOSPHOLIPASE; PROTEIN KEGG; PROTEIN PFAM; PROTEINASE; PROTEOME; SECRETOME; TRANSCRIPTOME; UNCLASSIFIED DRUG;

AGING; ARTICLE; ASEXUAL REPRODUCTION; ASPERGILLUS NIGER; AUTOPHAGY; CARBON METABOLISM; CELL DEATH; CELL DIFFERENTIATION; CELL INTERACTION; ENZYME RELEASE; FUNGAL STRUCTURES; FUNGUS CULTURE; FUNGUS GROWTH; GENETIC TRANSCRIPTION; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; SURVIVAL TIME;

ASPERGILLUS NIGER; AUTOPHAGY; BIOREACTORS; CARBON; FERMENTATION; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HYDROLASES; HYPHAE; MASS SPECTROMETRY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCTION, ASEXUAL; TRANSCRIPTOME;

ASPERGILLUS NIGER; FUNGI;

EID: 84864537150     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-380     Document Type: Article

References (71)

1. Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, Andersen MR, Bendtsen JD, Benen JA, van den Berg MA, Breestraat S, Caddick MX, Contreras R, Cornell M, Coutinho PM, Danchin EG, Debets AJ, Dekker P, van Dijck PW, van Dijk A, Dijkhuizen L, Driessen AJ, D'Enfert C, Geysens S, Goosen C, Groot GS, de Groot PW, Guillemette T, Henrissat B, Herweijer M, van den Hombergh JP, van der Heijden RT, van der Kaaij RM, Klis FM, Kools HJ, Kubicek CP, VanKuyk PA, Lauber J, Lu X, van der Maarel MJEC, Meulenberg R, Menke H, Mortimer MA, Nielsen J, Oliver SG, Olsthoorn M, Pal K, van Peij NN, Ram AFJ, Rinas U, Roubos JA, Sagt CM, Schmoll M, Sun J, Ussery D, Varga J, Vervecken W, van de Vondervoort PJ, Wedler H, Wosten HA, Zeng AP, van Ooyen AJ, Visser J, Stam H, . Hondel Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 2007, 25(2):221-231. 10.1038/nbt1282, 17259976, Hondel.
2. Andersen MR, Salazar MP, Schaap PJ, van der Vondervoort PJI, Culley D, Thykaer J, Frisvad JC, Nielsen KF, Albang R, Albermann K, Berka RM, Braus GH, Braus-stromeyer SA, Corrochano LM, Dai Z, Dijck PWMV, Hofmann G, Lasure LL, Magnuson JK, Menke H, Meijer M, Meijer SL, Nielsen JB, Nielsen ML, Ooyen AJJV, Pel HJ, Poulsen L, Samson RA, Stam H, Tsang A, Brink JMVD, Atkins A, Aerts A, Shapiro H, Pangilinan J, Salamov A, Lou Y, Lindquist E, Lucas S, Grimwood J, Grigoriev IV, Kubicek CP, Martinez D, Peij NMEV, Roubos JA, Nielsen J, Baker SE. Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing. Genome Res 2011, 21(6):885-897. 10.1101/gr.112169.110, 3106321, 21543515.
3. Archer DB. Filamentous fungi as microbial cell factories for food use. Curr opin biotechnol 2000, 11(5):478-83. 10.1016/S0958-1669(00)00129-4, 11024367.
4. Schuster E, Dunn-Coleman N, Frisvad JC, Van Dijck PWM. On the safety of Aspergillus niger-a review. Appl microbiol and biotechnol 2002, 59(4-5):426-35.
5. Pitt JI, Hocking AD. Fungi and Food Spoilage 1997, London: Blackie Academic and Professional.
6. Mogensen JM, Frisvad JC, Thrane U, Nielsen KF. Production of Fumonisin B2 and B4 by Aspergillus niger on grapes and raisins. J agric and food chem 2010, 58(2):954-8.
7. Person A, Chudgar SM, Norton BL, Tong BC, Stout JE. Aspergillus niger: an unusual cause of invasive pulmonary aspergillosis. J medical microbiol 2010, 59(Pt 7):834-8.
8. Adams TH, Wieser JK, Yu JH. Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 1998, 62:35-54. 98905, 9529886.
9. Broderick AJ, Greenshields RN. Sporulation of Aspergillus niger and Aspergillus ochraceus in Continuous Submerged Liquid Culture. Microbiology 1981, 126:193-202.
10. Schrickx JM, Krave AS, Verdoes JC, van den Hondel CAMJJ, Stouthamer AH, van Verseveld HW. Growth and product formation in chemostat and recycling cultures by Aspergillus niger N402 and a glucoamylase overproducing transformant, provided with multiple copies of the glaA gene. J gen microbiol 1993, 139(11):2801-10. 10.1099/00221287-139-11-2801, 8277260.
11. Jørgensen TR, Nitsche BM, Lamers GEM, Arentshorst M, van den Hondel CAMJJ, Ram AFJ. Transcriptomic insights into the physiology of Aspergillus niger approaching a specific growth rate of zero. Appl Environ Microbiol 2010, 76(16):5344-5355. 10.1128/AEM.00450-10, 2918955, 20562270.
12. White S, McIntyre M, Berry DR, McNeil B. The autolysis of industrial filamentous fungi. Crit Rev Biotechnol 2002, 22:1-14. 10.1080/07388550290789432, 11958333.
13. McNeil B, Berry DR, Harvey LM, Grant A, White S. Measurement of autolysis in submerged batch cultures of Penicillium chrysogenum. Biotechnol and Bioeng 1998, 57(3):297-305.
14. McIntyre M, Berry DR, McNeil B. Role of proteases in autolysis of Penicillium chrysogenum chemostat cultures in response to nutrient depletion. Appl Microbiol Biotechnol 2000, 53(2):235-242. 10.1007/s002530050014, 10709988.
15. Emri T, Molnár Z, Pusztahelyi T, Varecza Z, Pócsi I. The fluG-BrlA pathway contributes to the initialisation of autolysis in submerged Aspergillus nidulans cultures. Mycol Res 2005, 109(Pt 7):757-763.
16. Pusztahelyi T, Molnár Z, Emri T, Klement E, Miskei M, Kerékgyárto J, Balla J, Pócsi I. Comparative studies of differential expression of chitinolytic enzymes encoded by chiA, chiB, chiC and nagA genes in Aspergillus nidulans. Folia microbiologica 2006, 51(6):547-54. 10.1007/BF02931619, 17455791.
17. Hamann A, Brust D, Osiewacz HD. Apoptosis pathways in fungal growth, development and ageing. Trends Microbiol 2008, 16(6):276-283. 10.1016/j.tim.2008.03.003, 18440231.
18. Etxebeste O, Ugalde U, Espeso EA. Others: Adaptative and Developmental Responses to Stress in Aspergillus nidulans. Curr Protein and Pept Sci 2010, 11(8):704-718.
19. Emri T, Molnár Z, Szilágyi M, Pócsi I. Regulation of autolysis in Aspergillus nidulans. Appl biochem and biotechnol 2008, 151(2-3):211-20.
20. Lockshin RA, Zakeri Z. Apoptosis, autophagy, and more. int j biochem and cell biol 2004, 36(12):2405-19.
21. Giansanti V, Torriglia A, Scovassi AI. Conversation between apoptosis and autophagy: " Is it your turn or mine?" . Apoptosis : int j programmed cell death 2011, 16(4):321-33.
22. Edinger AL, Thompson CB. Death by design : apoptosis, necrosis and autophagy. Curr Opin Cell Biol 2004, 16:663-669. 10.1016/j.ceb.2004.09.011, 15530778.
23. Bos C, Debets A, Swart K, Huybers A. Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger. Curr genet 1988, 14(5):437-443. 10.1007/BF00521266, 3224384.
24. Hrdlicka PJ, Sørensen AB, Poulsen BR, Ruijter GJG, Visser J, Iversen JJL. Characterization of nerolidol biotransformation based on indirect on-line estimation of biomass concentration and physiological state in batch cultures of Aspergillus niger. Biotechnol prog 2004, 20:368-76.
25. Pollack JK, Li ZJ, Marten MR. Fungal mycelia show lag time before re-growth on endogenous carbon. Biotechnol and bioeng 2008, 100(3):458-65.
26. Emri T, Molnár Z, Veres T, Tünde P, Dudas G, Pócsi I. Glucose-mediated repression of autolysis and conidiogenesis in Emericella nidulans. Mycol Res 2006, 110(Pt 10):1172-1178.
27. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
28. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29. 10.1038/75556, 3037419, 10802651.
29. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer ELL, Studholme DJ, Yeats C, Eddy SR. The Pfam protein families database. Nucleic acids res 2004, 32(Database issue):138-41.
30. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic acids res 2010, 38(Database issue):D355-60. 2808910, 19880382.
31. Nitsche BM, Crabtree J, Cerqueira GC, Meyer V, Ram A, Wortman JR. New resources for functional analysis of omics data for the genus Aspergillus. BMC genomics 2011, 12:486. 10.1186/1471-2164-12-486, 3217955, 21974739.
32. Kuyk PAVAN, Diderich JA, Cabe APMAC, Hererro O, Ruijter GJG, Visser J. Aspergillus niger mstA encodes a high-affinity sugar/H+ symporter which is regulated in response to extracellular pH. Society 2004, 383:375-383.
33. Kelly DE, Krasevec N, Mullins J, Nelson DR. The CYPome (Cytochrome P450 complement) of Aspergillus nidulans. Fungal genet and biol 2009, 46(Suppl 1):S53-61.
34. Kanki T, Klionsky DJ, Okamoto K. Mitochondria autophagy in yeast. Antioxidants and redox signaling 2011, 14(10):1989-2001. 10.1089/ars.2010.3762, 3078492, 21194379.
35. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007, 9(10):1102-1109. 10.1038/ncb1007-1102, 17909521.
36. Xie Z, Nair U, Klionsky DJ. Atg8 Controls Phagophore Expansion during Autophagosome Formation. Mol Biol Cell 2008, 19(August):3290-3298. 2488302, 18508918.
37. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic acids res 2009, 37(Database issue):233-8.
38. Mattern IE, van Noort JM, van den Berg P, Archer DB, Roberts IN, van den Hondel CAMJJ. Isolation and characterization of mutants of Aspergillus niger deficient in extracellular proteases. Mol and gen genet: MGG 1992, 234(2):332-6.
39. Punt PJ, Schuren FHJ, Lehmbeck J, Christensen T, Hjort C, van den Hondel CAMJJ. Characterization of the Aspergillus niger prtT, a unique regulator of extracellular protease encoding genes. Fungal genet and biol 2008, 45(12):1591-9.
40. Miller KY, Toennis TM, Adams TH, Miller BL. Isolation and transcriptional characterization of a morphological modifier: the Aspergillus nidulans stunted (stuA) gene. Mol and gen genet: MGG 1991, 227(2):285-92.
41. Fischer R. Conidiation in Aspergillus nidulans. In Molecular Biology of Fungal Development 2002, 59-86. New York: Marcel Dekker, Osiewacz HD.
42. Emri T, Molnár Z, Pusztahelyi T, Pócsi I. Physiological and morphological changes in autolyzing Aspergillus nidulans cultures. Folia microbiologica 2004, 49(3):277-84. 10.1007/BF02931043, 15259768.
43. Braaksma M, Martens-Uzunova ES, Punt PJ, Schaap PJ. An inventory of the Aspergillus niger secretome by combining in silico predictions with shotgun proteomics data. BMC genomics 2010, 11:584. 10.1186/1471-2164-11-584, 3091731, 20959013.
44. Wösten HAB, Moukha SM, Sietsma JH, Wessels JG. Localization of growth and secretion of proteins in Aspergillus niger. J gen microbiol 1991, 137(8):2017-23. 10.1099/00221287-137-8-2017, 1955876.
45. Levin AM, de Vries RP, Conesa A, de Bekker C, Talon M, Menke HH, van Peij NNME, Wösten HAB. Spatial differentiation in the vegetative mycelium of Aspergillus niger. Eukaryotic cell 2007, 6(12):2311-22. 10.1128/EC.00244-07, 2168252, 17951513.
46. Krijgsheld P, Altelaar A, Post H, Ringrose JH, Müller WH, Heck AJR, Wösten HAB. Spatially resolving the secretome within the mycelium of the cell factory Aspergillus niger. J proteome res 2012, 11(5):2807-18. 10.1021/pr201157b, 22443316.
47. de Bekker C, van Veluw GJ, Vinck A, Wiebenga LA, Wösten HAB. Heterogeneity of Aspergillus niger microcolonies in liquid shaken cultures. Appl and environ microbiol 2011, 77(4):1263-7.
48. Emri T, Molnár Z, Pócsi I. The appearances of autolytic and apoptotic markers are concomitant but differently regulated in carbon-starving Aspergillus nidulans cultures. FEMS microbiol lett 2005, 251(2):297-303. 10.1016/j.femsle.2005.08.015, 16165325.
49. Agger T, Spohr AB, Carlsen M, Nielsen J. Growth and product formation of Aspergillus oryzae during submerged cultivations: verification of a morphologically structured model using fluorescent probes. Biotechnol and bioeng 1998, 57(3):321-9.
50. Müller C, Spohr AB, Nielsen J. Role of substrate concentration in mitosis and hyphal extension of Aspergillus. Biotechnol and bioeng 2000, 67(4):390-7.
51. Shoji JY, Arioka M, Kitamoto K. Possible involvement of pleiomorphic vacuolar networks in nutrient recycling in filamentous fungi. Autophagy 2006, 2(3):226-7.
52. Kikuma T, Arioka M, Kitamoto K. Autophagy during conidiation and conidial germination in filamentous fungi. Autophagy 2007, 3(2):128-9.
53. Kanki T, Klionsky DJ. Mitophagy in yeast occurs through a selective mechanism. J Biol Chem 2008, 283(47):32386-32393. 10.1074/jbc.M802403200, 2583303, 18818209.
54. Kimura S, Maruyama JI, Kikuma T, Arioka M, Kitamoto K. Autophagy delivers misfolded secretory proteins accumulated in endoplasmic reticulum to vacuoles in the filamentous fungus Aspergillus oryzae. Biochem and biophys res commun 2011, 406(3):464-70.
55. Moukha SM, Wösten HAB, Asther M, Wessels JG. In situ localization of the secretion of lignin peroxidases in colonies of Phanerochaete chrysosporium using a sandwiched mode of culture. J gen microbiol 1993, 139(5):969-78. 10.1099/00221287-139-5-969, 8336112.
56. Vishniac W, Santer M. The thiobacilli. Bacteriological rev 1957, 21(3):195-213.
57. Braaksma M, Smilde AK, van der Werf MJ, Punt PJ. The effect of environmental conditions on extracellular protease activity in controlled fermentations of Aspergillus niger. Microbiol (Reading, England) 2009, 155(Pt 10):3430-9.
58. Abràmoff MD, Hospitals I, Magalhães PJ. Image Processing with ImageJ. Medicine 2004, 11(7):36-42.
59. Damveld RA, Arentshorst M, Franken A, VanKuyk PA, Klis FM, van den Hondel CAMJJ, Ram AFJ. The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol Microbiol 2005, 58:305-319. 10.1111/j.1365-2958.2005.04827.x, 16164567.
60. R-Team R: A Language and Environment for Statistical Computing 2008, Vienna, Austria: R Foundation for Statistical Computing, R-Team.
61. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry RA, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5(10):R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
62. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20(3):307-315. 10.1093/bioinformatics/btg405, 14960456.
63. MacDonald JW. affycoretools: Functions useful for those doing repetitive analyses with Affymetrix GeneChips. 2008,
64. Bolstad BM, Collin F, Brettschneider J, Simpson K, Cope L, Irizarry RA, Speed TP. Quality assessment of affymetrix genechip data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005-2005. New York: Springer.
65. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003, 31(4):e15. 10.1093/nar/gng015, 150247, 12582260.
66. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall K, Phillippy KH, Sherman PM, Muertter RN, Holko M, Ayanbule O, Yefanov A, Soboleva A. NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic acids res 2011, 39(Database issue):D1005-10. 3013736, 21097893.
67. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B (Methodological) 1995, 57:289-300.
68. van den Berg RA, Braaksma M, van der Veen D, van der Werf MJ, Punt PJ, van der Oost J, de Graaff LH. Identification of modules in Aspergillus niger by gene co-expression network analysis. Fungal Genet Biol 2010, 47(6):539-50. 10.1016/j.fgb.2010.03.005, 20350613.
69. van den Berg RA, Hoefsloot HCJ, Westerhuis JA, Smilde AK, van der Werf MJ. Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC genomics 2006, 7:142. 10.1186/1471-2164-7-142, 1534033, 16762068.
70. Thakur SS, Geiger T, Chatterjee B, Bandilla P, Fröhlich F, Cox J, Mann M. Deep and Highly Sensitive Proteome Coverage by LC-MS/MS Without Prefractionation. Mol and cell proteomics : MCP 2011, 10(8):M110.003699.
71. Lu P, Vogel C, Wang R, Yao X, Marcotte EM. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat biotechnol 2007, 25:117-24. 10.1038/nbt1270, 17187058.