Identification of the novel penicillin biosynthesis gene aatB of Aspergillus nidulans and its putative evolutionary relationship to this fungal secondary metabolism gene cluster

Molecular Microbiology

Volumn 70, Issue 2, 2008, Pages 445-461

  Spröte, Petra ^a,b   Hynes, Michael J ^c   Hortschansky, Peter ^a,b   Shelest, Ekaterina ^a   Scharf, Daniel H ^a,b   Wolke, Sandra M ^a,b   Brakhage, Axel A ^a,b  

^a HANS KNÖLL INSTITUTE   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PENICILLIN G; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ANBH1F; TRANSCRIPTION FACTOR ANCF; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS NIDULANS; BIOSYNTHESIS; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE STRUCTURE; GENOME; MOLECULAR EVOLUTION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; SURFACE PLASMON RESONANCE; WILD TYPE;

ACYLTRANSFERASES; AMINO ACID SEQUENCE; ANIMALS; ASPERGILLUS NIDULANS; BLOTTING, NORTHERN; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION PROFILING; GENE ORDER; GENES, FUNGAL; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; PENICILLIN-BINDING PROTEINS; PENICILLINS; PHYLOGENY; PROTEIN SORTING SIGNALS; SEQUENCE HOMOLOGY, AMINO ACID; SURFACE PLASMON RESONANCE; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); EMERICELLA NIDULANS; FUNGI;

EID: 52649133438     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06422.x     Document Type: Article

References (59)

1. Aharonowitz, Y., Cohen, G. Martin, J.F. (1992) Penicillin and cephalosporin biosynthetic genes: structure, organization, regulation, and evolution. Annu Rev Microbiol 46 : 461 495.
2. Alvarez, E., Meesschaert, B., Montenegro, E., Gutierrez, S., Diez, B., Barredo, J.L. Martin, J.F. (1993) The isopenicillin-N acyltransferase of Penicillium chrysogenum has isopenicillin-N amidohydrolase, 6-aminopenicillanic acid acyltransferase and penicillin amidase activities, all of which are encoded by the single penDE gene. Eur J Biochem 215 : 323 332.
3. Ballance, D.J. Turner, G. (1985) Development of a high-frequency transforming vector for Aspergillus nidulans. Gene 36 : 321 331.
4. Barredo, J.L., van Solingen, P., Diez, B., Alvarez, E., Cantoral, J.M., Kattevilder, A., et al. (1989) Cloning and characterization of the acyl-coenzyme A: 6-aminopenicillanic-acid-acyltransferase gene of Penicillium chrysogenum. Gene 83 : 291 300.
5. Bergmann, S., Schumann, J., Scherlach, K., Lange, C., Brakhage, A.A. Hertweck, C. (2007) Genomics-driven discovery of PKS-NRPS hybrid metabolites from Aspergillus nidulans. Nat Chem Biol 3 : 213 217.
6. Bok, J.W. Keller, N.P. (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3 : 527 535.
7. Brakhage, A.A. (1998) Molecular regulation of beta-lactam biosynthesis in filamentous fungi. Microbiol Mol Biol Rev 62 : 547 585.
8. Brakhage, A.A. (1999) Biosynthesis of beta-lactam compounds in microorganisms. In Amino Acids, Peptides, Pophyrins and Alkaloids, Vol. 4. Kelly, J.W. (ed.). Amsterdam : Elsevier Science, pp. 159 193.
9. Brakhage, A.A. Van den Brulle, J. (1995) Use of reporter genes to identify recessive trans-acting mutations specifically involved in the regulation of Aspergillus nidulans penicillin biosynthesis genes. J Bacteriol 177 : 2781 2788.
10. Brakhage, A.A., Browne, P. Turner, G. (1992) Regulation of Aspergillus nidulans penicillin biosynthesis and penicillin biosynthesis genes acvA and ipnA by glucose. J Bacteriol 174 : 3789 3799.
11. Brakhage, A.A., Spröte, P., Al-Abdallah, Q., Gehrke, A., Plattner, H. Tüncher, A. (2004) Regulation of penicillin biosynthesis in filamentous fungi. Adv Biochem Eng Biotechnol 88 : 45 90.
12. Brakhage, A.A., Al-Abdallah, Q., Tüncher, A. Spröte, P. (2005) Evolution of beta-lactam biosynthesis genes and recruitment of trans-acting factors. Phytochemistry 66 : 1200 1210.
13. Brocard, C. Hartig, A. (2006) Peroxisome targeting signal 1: is it really a simple tripeptide? Biochim Biophys Acta 1763 : 1565 1573.
14. Caruso, M.L., Litzka, O., Martic, G., Lottspeich, F. Brakhage, A.A. (2002) Novel basic-region helix-loop-helix transcription factor (AnBH1) of Aspergillus nidulans counteracts the CCAAT-binding complex AnCF in the promoter of a penicillin biosynthesis gene. J Mol Biol 323 : 425 439.
15. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G. Thompson, J.D. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31 : 3497 3500.
16. Espeso, E.A., Tilburn, J., Arst, H.N., Jr. Peñalva, M.A. (1993) pH regulation is a major determinant in expression of a fungal penicillin biosynthetic gene. EMBO J 12 : 3947 3956.
17. Galagan, J.E., Calvo, S.E., Cuomo, C., Ma, L.J., Wortman, J.R., Batzoglou, S., et al. 2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438 : 1105 1115.
18. Haarmann, T., Machado, C., Lubbe, Y., Correia, T., Schardl, C.L., Panaccione, D.G. Tudzynski, P. (2005) The ergot alkaloid gene cluster in Claviceps purpurea: extension of the cluster sequence and intra species evolution. Phytochemistry 66 : 1312 1320.
19. Herrmann, M., Spröte, P. Brakhage, A.A. (2006) Protein kinase C (PkcA) of Aspergillus nidulans is involved in penicillin production. Appl Environ Microbiol 72 : 2957 2970.
20. Hortschansky, P., Eisendle, M., Al-Abdallah, Q., Schmidt, A.D., Bergmann, S., Thön, M., et al. (2007) Interaction of HapX with the CCAAT-binding complex - a novel mechanism of gene regulation by iron. EMBO J 26 : 3157 3168.
21. Hughes, A.L. Friedman, R. (2007) Sharing of transcription factors after gene duplication in the yeast Saccharomyces cerevisiae. Genetica 129 : 301 308.
22. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G. Gibson, T.J. (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23 : 403 405.
23. Keller, N.P. Hohn, T.M. (1997) Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21 : 17 29.
24. Khaldi, N., Collemare, J., Lebrun, M.H. Wolfe, K.H. (2008) Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9 : R18.
25. Landan, G., Cohen, G., Aharonowitz, Y., Shuali, Y., Graur, D. Shiffman, D. (1990) Evolution of isopenicillin N synthase genes may have involved horizontal gene transfer. Mol Biol Evol 7 : 399 406.
26. Lawrence, J.G. Roth, J.R. (1996) Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143 : 1843 1860.
27. Lee, S. Taylor, J. (1990) Isolation of DNA from fungal mycelia and single spores. In PCR Protocols: A Guide to Methods and Applications. Innis, M.A., Gelfand, D.H. White, T.J. (eds). San Diego, CA : Academic Press, pp. 282 287.
28. Litzka, O., Then Bergh, K. Brakhage, A.A. (1996) The Aspergillus nidulans penicillin-biosynthesis gene aat (penDE) is controlled by a CCAAT-containing DNA element. Eur J Biochem 238 : 675 682.
29. Litzka, O., Papagiannopolous, P., Davis, M.A., Hynes, M.J. Brakhage, A.A. (1998) The penicillin regulator PENR1 of Aspergillus nidulans is a HAP-like transcriptional complex. Eur J Biochem 251 : 758 767.
30. Louis, E.J. (2007) Evolutionary genetics: making the most of redundancy. Nature 449 : 673 674.
31. Lynch, M. Force, A. (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154 : 459 473.
32. Mantovani, R. (1998) A survey of 178 NF-Y binding CCAAT boxes. Nucleic Acids Res 26 : 1135 1143.
33. Marchler-Bauer, A. Bryant, S.H. (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32 : W327 W331.
34. Monahan, B.J., Askin, M.C., Hynes, M.J. Davis, M.A. (2006) Differential expression of Aspergillus nidulans ammonium permease genes is regulated by GATA transcription factor AreA. Eukaryot Cell 5 : 226 237.
35. Müller, W.H., Bovenberg, R.A., Groothuis, M.H., Kattevilder, F., Smaal, E.B., Van der Voort, L.H. Verkleij, A.J. (1992) Involvement of microbodies in penicillin biosynthesis. Biochim Biophys Acta 1116 : 210 213.
36. Nayak, T., Szewczyk, E., Oakley, C.E., Osmani, A., Ukil, L., Murray, S.L., et al. (2006) A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172 : 1557 1566.
37. van Noort, V., Snel, B. Huynen, M.A. (2004) The yeast coexpression network has a small-world, scale-free architecture and can be explained by a simple model. EMBO Rep 5 : 280 284.
38. Peñalva, M.A., Moya, A., Dopazo, J. Ramon, D. (1990) Sequences of isopenicillin N synthetase genes suggest horizontal gene transfer from prokaryotes to eukaryotes. Proc Biol Sci 241 : 164 169.
39. Pontecorvo, G., Roper, J.A., Hemmons, L.M., Macdonald, K.D. Bufton, A.W. (1953) The genetics of Aspergillus nidulans. Adv Genet 5 : 141 238.
40. Proctor, R.H., Brown, D.W., Plattner, R.D. Desjardins, A.E. (2003) Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet Biol 38 : 237 249.
41. Rosenthal, H.E. (1967) A graphic method for the determination and presentation of binding parameters in a complex system. Anal Biochem 20 : 525 532.
42. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
43. Schmitt, E.K., Hoff, B. Kück, U. (2004) Regulation of cephalosporin biosynthesis. Adv Biochem Eng Biotechnol 88 : 1 43.
44. Shwab, E.K., Bok, J.W., Tribus, M., Galehr, J., Graessle, S. Keller, N.P. (2007) Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot Cell 6 : 1656 1664.
45. Siemieniewicz, K.W. Schrempf, H. (2007) Concerted responses between the chitin-binding protein secreting Streptomyces olivaceoviridis and Aspergillus proliferans. Microbiology 153 : 593 600.
46. Skatrud, P.L. (1991) Molecular biology of the beta-lactam-producing fungi. In More Gene Manipulations in Fungi. Bennett, J.W. Lasure, L.L. (eds). New York : Academic Press, pp. 364 395.
47. Smith, D.J., Burnham, M.K., Bull, J.H., Hodgson, J.E., Ward, J.M., Browne, P., et al. (1990a) Beta-lactam antibiotic biosynthetic genes have been conserved in clusters in prokaryotes and eukaryotes. EMBO J 9 : 741 747.
48. Smith, D.J., Burnham, M.K., Edwards, J., Earl, A.J. Turner, G. (1990b) Cloning and heterologous expression of the penicillin biosynthetic gene cluster from Penicillum chrysogenum. Biotechnology (NY) 8 : 39 41.
49. Spröte, P. Brakhage, A.A. (2007) The light-dependent regulator velvet A of Aspergillus nidulans acts as a repressor of the penicillin biosynthesis. Arch Microbiol 188 : 69 79.
50. Steidl, S., Papagiannopoulos, P., Litzka, O., Andrianopoulos, A., Davis, M.A., Brakhage, A.A. Hynes, M.J. (1999) AnCF, the CCAAT binding complex of Aspergillus nidulans, contains products of the hapB, hapC, and hapE genes and is required for activation by the pathway-specific regulatory gene amdR. Mol Cell Biol 19 : 99 106.
51. Teichmann, S.A. Babu, M.M. (2004) Gene regulatory network growth by duplication. Nat Genet 36 : 492 496.
52. Then Bergh, K., Litzka, O. Brakhage, A.A. (1996) Identification of a major cis-acting DNA element controlling the bidirectionally transcribed penicillin biosynthesis genes acvA (pcbAB) and ipnA (pcbC) of Aspergillus nidulans. J Bacteriol 178 : 3908 3916.
53. Tilburn, J., Sarkar, S., Widdick, D.A., Espeso, E.A., Orejas, M., Mungroo, J., et al. (1995) The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. EMBO J 14 : 779 790.
54. Tobin, M.B., Fleming, M.D., Skatrud, P.L. Miller, J.R. (1990) Molecular characterization of the acyl-coenzyme A: isopenicillin N acyltransferase gene (penDE) from Penicillium chrysogenum and Aspergillus nidulans and activity of recombinant enzyme in Escherichia coli. J Bacteriol 172 : 5908 5914.
55. Todd, R.B., Davis, M.A. Hynes, M.J. (2007) Genetic manipulation of Aspergillus nidulans: meiotic progeny for genetic analysis and strain construction. Nat Protoc 2 : 811 821.
56. Tudzynski, B. (2005) Gibberellin biosynthesis in fungi: genes, enzymes, evolution, and impact on biotechnology. Appl Microbiol Biotechnol 66 : 597 611.
57. Valiante, V., Heinekamp, T., Jain, R., Härtl, A. Brakhage, A.A. (2008) The mitogen-activated protein kinase MpkA of Aspergillus fumigatus regulates cell wall signaling and oxidative stress response. Fungal Genet Biol 45 : 618 627.
58. Walton, J.D. (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 30 : 167 171.
59. TM Yeast DNA purification kit. Epicentre Forum 11 : 7.