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Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88

Title:

Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88

Andersen, M. R. and Salazar, M. P. and Schaap, P. J. and van de Vondervoort, P. J. I. and Culley, D. and Thykaer, J. and Frisvad, J. C. and Nielsen, K. F. and Albang, R. and Albermann, K. and Berka, R. M. and Braus, G. H. and Braus-Stromeyer, S. A. and Corrochano, L. M. and Dai, Z. and van Dijck, P. W. M. and Hofmann, G. and Lasure, L. L. and Magnuson, J. K. and Menke, H. and Meijer, M. and Meijer, S. L. and Nielsen, J. B. and Nielsen, M. L. and van Ooyen, A. J. J. and Pel, H. J. and Poulsen, L. and Samson, R. A. and Stam, H. and Tsang, Adrian and van den Brink, J. M. and Atkins, A. and Aerts, A. and Shapiro, H. and Pangilinan, J. and Salamov, A. and Lou, Y. and Lindquist, E. and Lucas, S. and Grimwood, J. and Grigoriev, I. V. and Kubicek, C. P. and Martinez, D. and van Peij, N. N. M. E. and Roubos, J. A. and Nielsen, J. and Baker, S. E. (2011) Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88. Genome Research, 21 (6). pp. 885-897. ISSN 1088-9051

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Official URL: http://dx.doi.org/10.1101/gr.112169.110

Abstract

The filamentous fungus Aspergillus niger exhibits great diversity in its phenotype. It is found globally, both as marine and terrestrial strains, produces both organic acids and hydrolytic enzymes in high amounts, and some isolates exhibit pathogenicity. Although the genome of an industrial enzyme-producing A. niger strain (CBS 513.88) has already been sequenced, the versatility and diversity of this species compel additional exploration. We therefore undertook whole-genome sequencing of the acidogenic A. niger wild-type strain (ATCC 1015) and produced a genome sequence of very high quality. Only 15 gaps are present in the sequence, and half the telomeric regions have been elucidated. Moreover, sequence information from ATCC 1015 was used to improve the genome sequence of CBS 513.88. Chromosome-level comparisons uncovered several genome rearrangements, deletions, a clear case of strain-specific horizontal gene transfer, and identification of 0.8 Mb of novel sequence. Single nucleotide polymorphisms per kilobase (SNPs/kb) between the two strains were found to be exceptionally high (average: 7.8, maximum: 160 SNPs/kb). High variation within the species was confirmed with exo-metabolite profiling and phylogenetics. Detailed lists of alleles were generated, and genotypic differences were observed to accumulate in metabolic pathways essential to acid production and protein synthesis. A transcriptome analysis supported up-regulation of genes associated with biosynthesis of amino acids that are abundant in glucoamylase A, tRNA-synthases, and protein transporters in the protein producing CBS 513.88 strain. Our results and data sets from this integrative systems biology analysis resulted in a snapshot of fungal evolution and will support further optimization of cell factories based on filamentous fungi.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Refereed:Yes
Authors:Andersen, M. R. and Salazar, M. P. and Schaap, P. J. and van de Vondervoort, P. J. I. and Culley, D. and Thykaer, J. and Frisvad, J. C. and Nielsen, K. F. and Albang, R. and Albermann, K. and Berka, R. M. and Braus, G. H. and Braus-Stromeyer, S. A. and Corrochano, L. M. and Dai, Z. and van Dijck, P. W. M. and Hofmann, G. and Lasure, L. L. and Magnuson, J. K. and Menke, H. and Meijer, M. and Meijer, S. L. and Nielsen, J. B. and Nielsen, M. L. and van Ooyen, A. J. J. and Pel, H. J. and Poulsen, L. and Samson, R. A. and Stam, H. and Tsang, Adrian and van den Brink, J. M. and Atkins, A. and Aerts, A. and Shapiro, H. and Pangilinan, J. and Salamov, A. and Lou, Y. and Lindquist, E. and Lucas, S. and Grimwood, J. and Grigoriev, I. V. and Kubicek, C. P. and Martinez, D. and van Peij, N. N. M. E. and Roubos, J. A. and Nielsen, J. and Baker, S. E.
Journal or Publication:Genome Research
Date:04 May 2011
ID Code:7715
Deposited By:DANIELLE DENNIE
Deposited On:11 Jul 2011 10:33
Last Modified:11 Jul 2011 10:33
References:
Abarca ML, Bragulat MR, Castella G, Cabanes FJ. 1994. Ochratoxin A production by strains of Aspergillus niger var. niger. Appl Environ Microbiol 60: 2650–2652.

Alexa A, Rahnenführer J, Lengauer T. 2006. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600–1607.

Andersen MR, Nielsen M, Nielsen J. 2008a. Metabolic model integration of the bibliome, genome, metabolome and reactome of Aspergillus niger. Mol Syst Biol 4: 178. doi: 10.1038/msb.2008.12.

Andersen MR, Vongsangnak W, Panagiotou G, Salazar M, Lehmann L, Nielsen J. 2008b. A tri-species Aspergillus micro array: Comparative transcriptomics of three Aspergillus species. Proc Natl Acad Sci 105: 4387–4392.

Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM, Dehal P, Christoffels A, Rash S, Hoon S, Smit A, et al. 2002. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297: 1301–1310.

Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25–29.

Baker SE. 2006. Aspergillus niger genomics: Past, present and into the future. Med Mycol Suppl 1 44: S17–S21.

Birney E, Durbin R. 2000. Using GeneWise in the Drosophila annotation experiment. Genome Res 10: 547–548.

Bos CJ, Debets AJ, Kobus G, Slakhorst SM, Swart K. 1989. Adenine and pyrimidine genes of Aspergillus niger and evidence for a seventh linkage group. Curr Genet 16: 307–310.

Braumann I, van den Berg M, Kempken F. 2008. Strain-specific retrotransposon-mediated recombination in commercially used Aspergillus niger strain. Mol Genet Genomics 280: 319–325.

Büchi G, Klaubert D, Shank R, Weinreb S, Wogan GN. 1971. Structure and synthesis of kotanin and desmethylkotanin, metabolites of Aspergillus glaucus. J Org Chem 36: 1143–1147.

Christias C, Couvaraki C, Georgopoulos SG, Vomvoyanni V. 1975. Protein content and amino acid composition of certain fungi evaluated for microbial protein production. Appl Microbiol 29: 250–254.

Cullen D. 2007. The genome of an industrial workhorse. Nat Biotechnol 25: 189–190.

Cuomo CA, Güldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M, et al. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400–1402.

Cutler HG, Crumley FG, Cox RH, Hernandez O, Cole RJ, Dorner JW. 1979. Orlandin: a nontoxic fungal metabolite with plant growth inhibiting properties. J Agric Food Chem 27: 592–595.

Debets A, Swart K, Bos C. 1989. Mitotic mapping in linkage group V of Aspergillus niger based on selection of auxotrophic recombinants by Novozym enrichment. Can J Microbiol 35: 982–988.

Debets A, Holub E, Swart K, van den Broek H, Bos C. 1990a. An electrophoretic karyotype of Aspergillus niger. Mol Gen Genet 224: 264–268.

Debets A, Swart K, Bos C. 1990b. Genetic analysis of Aspergillus niger: Isolation of chlorate resistance mutants, their use in mitotic mapping and evidence for an eighth linkage group. Mol Gen Genet 221: 453–458.

Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, et al. 2008. Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4: e1000046. doi: 10.1371/journal.pgen.1000046.

Frisvad JC, Samson R. 2004. Polyphasic taxonomy of Penicillium subgenus Penicillium. A guide to identification of the food and air-borne terverticillate Penicillia and their mycotoxins. Stud Mycol 49: 1–52.

Frisvad JC, Thrane U. 1987. Standardized high performance liquid chromatography of 182 mycotoxins and other fungal metabolites based on alkylphenone indices and UV VIS spectra (diode array detection). J Chromatogr 404: 195–214.

Frisvad JC, Larsen TO, de Vries R, Meijer M, Houbraken J, Cabañes FJ, Ehrlich K, Samson RA. 2007a. Secondary metabolite profiling, growth profiles and other tools for species recognition and important Aspergillus mycotoxins. Stud Mycol 59: 31–37.

Frisvad JC, Smedsgaard J, Samson R, Larsen T, Thrane U. 2007b. Fumonisin B2 production by Aspergillus niger. J Agric Food Chem 55: 9727–9732.

Fukuda T, Hasegawa Y, Hagimori K, Yamaguchi Y, Masuma R, Tomoda H, Omura S. 2006. Tensidols, new potentiators of antifungal miconazole activity, produced by Aspergillus niger FKI-2342. J Antibiot (Tokyo) 59: 480–485.

Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Baştürkmen M, Spevak CC, Clutterbuck J, et al. 2005. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105–1115.

Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. 2004. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5: R80. doi: 10.1186/gb-2004-5-10-r80.

Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61: 1323–1330.

Gordon D, Abajian C, Green P. 1998. Consed: A graphical tool for sequence finishing. Genome Res 8: 195–202.

Gottschling D, Aparicio O, Billington B, Zakian V. 1990. Position effect at S. cerevisiae telomeres: Reversible repression of Pol II transcription. Cell 63: 751–762.

Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, et al. 2004. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 1: D258–D261.

Hiort J, Maksimenka K, Reichert M, Perović-Ottstadt S, Lin WH, Wray V, Steube K, Schaumann K, Weber H, Proksch P, et al. 2004. New natural products from the sponge-derived fungus Aspergillus niger. J Nat Prod 67: 1532–1543.

Inokoshi J, Shiomi K, Masuma R, Tanaka H, Yamada H, Omura S. 1999. Funalenone, a novel collagenase inhibitor produced by Aspergillus niger. J Antibiot (Tokyo) 52: 1095–1100.

Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249–264.

Isogai A, Horii T, Suzuki A, Murakoshi S, Ikeda K, Sato S, Tamura S. 1975. Isolation and identification of nigragillin as an insecticidal metabolite produced by Aspergillus niger. Agric Biol Chem 39: 739–740

Kanehisa M, Guto S, Kawashima S, Nakaya A. 2002. The KEGG databases at GenomeNet. Nucleic Acids Res 30: 42–46.

Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Res 32: D277–D280.

Karaffa L, Kubicek CP. 2003. Aspergillus niger citric acid accumulation: do we understand this well working black box? Appl Microbiol Biotechnol 61: 189–196.

Keeling PJ, Palmer JD. 2008. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9: 605–617.

Khaldi N, Wolfe KH. 2008. Elusive origins of the extra genes in Aspergillus oryzae. PLoS ONE 3: e3036. doi: 10.1371/journal.pone.0003036.

Khaldi N, Collemare J, Lebrun MH, Wolfe KH. 2008. Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9: R18. doi: 10.1186/gb-2008-9-1-r18.

Koonin EV, Fedorova ND, Jackson JD, Jacobs AR, Krylov DM, Makarova KS, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, et al. 2004. A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol 5: R7. doi: 10.1186/gb-2004-5-2-r7.

Korman DR, Bayliss FT, Barnett CC, Carmona CL, Kodama KH, Royer TJ, Thompson SA, Ward M, Wilson LJ, Berka RM. 1990. Cloning, characterization, and expression of two alpha-amylase genes from Aspergillus niger var. awamori. Curr Genet 17: 203–212.

Kozakiewicz Z, Frisvad JC, Hawksworth DL, Pitt JI, Samson RA, Stolk AC. 1992. Proposals for nomina specifica conservanda and rijicienda in Aspergillus and Penicillium (Fungi). Taxon 41: 109–113.

Lubertozzi D, Keasling JD. 2008. Developing Aspergillus as a host for heterologous expression. Biotechnol Adv 27: 53–75.Medline↵Martens-Uzunova ES, Schaap PJ
Martens-Uzunova ES, Schaap PJ. 2008. An evolutionary conserved D-galacturonic acid metabolic pathway operates across filamentous fungi capable of pectin degradation. Fungal Genet Biol 45: 1449–1457.

McCleary BV, Bouhet F, Driguez H. 1991. Measurement of amyloglucosidase using p-nitrophenyl b-maltoside as substrate. Biotechnol Tech 5: 255–258.

McGinnis S, Madden T. 2004. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32: W20–W25.

Nielsen KF, Smedsgaard J. 2003. Fungal metabolite screening: database of 474 mycotoxins and fungal metabolites for dereplication by standardized liquid chromatography-UV-mass spectrometry methodology. J Chromatogr A 1002: 111–136.

Nielsen J, Villadsen J, Liden G. 2003. Bioreaction engineering principles, 2nd ed. Kluwer Academic/Plenum, New York.

Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, et al. 2007. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25: 221–231.

Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics methods and protocols: Methods in molecular biology (ed. Krawetz S, Misener S), pp. 365–386. Humana, Totowa,

Salamov AA, Solovyev VV. 2000. Ab initio gene finding in Drosophila genomic DNA. Genome Res 10: 516–522.

Schuster E, Dunn-Coleman N, Frisvad JC, van Dijck PWM. 2002. On the safety of Aspergillus niger—a review. Appl Microbiol Biotechnol 59: 426–435.

Shibuya I, Tamura G, Ishikawa T, Hara S. 1992. Cloning the alpha-amylase cDNA of Aspergillus shirousamii and its expression in Saccharomyces cerevisiae. Biosci Biotechnol Biochem 56: 174–179.

Smedsgaard J. 1997. Micro-scale extraction procedure for standardised screening of fungal metabolite production in cultures. J Chromatogr A 760: 264–270.

Strand DJ, McDonald JF. 1985. Copia is transcriptionally responsive to environmental stress. Nucleic Acids Res 13: 4401–4410.

Sun J, Lu X, Rinas U, Zeng A. 2007. Metabolic peculiarities of Aspergillus niger disclosed by comparative metabolic genomics. Genome Biol 8: R182. doi: 10.1186/gb-2007-8-9-r182.

Swart K, Debets AJ, Kobus G, Bos CJ. 1992. Arginine and proline genes of Aspergillus niger. Antonie van Leeuwenhoek 61: 259–264.

Tanaka H, Wang PL, Yamada O, Tamura L. 1966. Yellow pigments of Aspergillus niger and Asp. awamori. Part. I. Isolation of aurasperone A and related pigments. Agric Biol Chem 30: 107–113

van de Peer Y, de Wachter R. 1994. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10: 569–570.

van Dijck PWM. 2008. The importance of Aspergilli and regulatory aspects of Aspergillus nomenclature. In Aspergillus in the genomic era (ed. Varga J, Samso RA), pp. 249–257. Wageningen Academic, Wageningen, The Netherlands

van Dijck PWM, Selten GCM, Hempenius RA. 2003. On the safety of a new generation of DSM Aspergillus niger production strains. Regul Toxicol Pharmacol 38: 27–35.

van Lanen JM, Smith MB. 1968. Process of producing glucamylase and an alcohol product. US patent 3,418,211. Hiram Walker & Sons, Inc., Peoria, IL

Verdoes JC, Calil MR, Punt PJ, Debets F, Swart K, Stouthamer AH, van den Hondel CA. 1994. The complete karyotype of Aspergillus niger: The use of introduced electrophoretic mobility variation of chromosomes for gene assignment studies. Mol Gen Genet 244: 75–80.

Yuan X, Roubos J, van den Hondel C, Ram A. 2008a. Identification of InuR, a new Zn(II)2Cys6 transcriptional activator involved in the regulation of inulinolytic genes in Aspergillus niger. Mol Genet Genomics 279: 11–26.

Yuan XL, van der Kaaij RM, van den Hondel CA, Punt PJ, van der Maarel MJ, Dijkhuizen L, Ram AF. 2008b. Aspergillus niger genome-wide analysis reveals a large number of novel α-glucan acting enzymes with unexpected expression profiles. Mol Genet Genomics 279: 545–561.

Zdobnov EM, Apweiler R. 2001. InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847–848.
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