Abstract
Starting from three amino acid precursors, penicillin biosynthesis is catalyzed by three enzymes which are encoded by the following three genes: acvA (pcbAB), ipnA (pcbC), and aat (penDE). To identify trans-acting mutations which are specifically involved in the regulation of these secondary metabolism genes, a molecular approach was employed by using an Aspergillus nidulans strain (AXTII9) carrying acvA-uidA and ipnA-lacZ gene fusions integrated in double copies at the chromosomal argB gene. On minimal agar plates supplemented with X-Gal (5-bromo-4-chloro-3-indolyl-beta-D-galactopyranoside), colonies of such a strain stained blue, which is indicative of ipnA-lacZ expression. After mutagenesis with UV light, colonies were isolated on agar plates with lactose as the carbon source, which produced only a faint blue color or no color at all. Such mutants (named Prg for penicillin regulation) most likely were defective in trans-acting genes. Control experiments revealed that the mutants studied still carried the correct number of gene fusions. In a fermentation run, mutants Prg-1 and Prg-6 exhibited only 20 to 50% of the ipnA-lacZ expression of the wild-type strain and produced only 20 to 30% of the penicillin produced by the wild-type strain. Western blot (immunoblot) analysis showed that these mutants contained reduced amounts of ipnA gene product, i.e., isopenicillin N synthase. Both mutant Prg-1 and mutant Prg-6 also differed in acvA-uidA expression levels from the wild type. Segregation analysis indicated that for both mutants the Prg phenotype resulted from mutation of a single gene. Two different complementation groups, which were designated prgA1 and prgB1, were identified. However, the specific activity of the aat (penDE) gene product, i.e., acyl coenzyme A:6-aminopenicillanic acid acyltransferase, was essentially the same for the mutants as for the wild-type strain, implying that the last step of the penicillin biosynthetic pathway is not affected by the trans-acting mutations identified.
MeSH Terms
Acyltransferases/analysis
Aspergillus nidulans/enzymology,genetics
Crosses, Genetic
Fermentation
Galactosides/metabolism
Gene Expression Regulation, Fungal
Genes, Recessive
Genes, Reporter
Genetic Complementation Test
Indoles/metabolism
Lac Operon
Mutagenesis
Oxidoreductases/genetics
Penicillin-Binding Proteins
Penicillins/biosynthesis
Recombinant Fusion Proteins/biosynthesis
Selection, Genetic
Transcriptional Activation
Chemicals
Galactosides
Indoles
Penicillin-Binding Proteins
Penicillins
Recombinant Fusion Proteins
Oxidoreductases
isopenicillin N synthetase
Acyltransferases
acyl-CoA-6-aminopenicillanic acid acyltransferase
5-bromo-4-chloro-3-indolyl beta-galactoside
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Brakhage A A
Lehrstuhl für Mikrobiologie, Universität München, Federal Republic of Germany.
Van den Brulle J
References (33)
33 references, click to expand
-
Molecular biology of penicillin and cephalosporin biosynthesis.
Antimicrob Agents Chemother. 1990 Jun;34(6):943-8
PMID: 2203307
-
Genetic regulation of development in Aspergillus nidulans.
Trends Genet. 1988 Jun;4(6):162-9
PMID: 3076298
-
Regulation of Aspergillus nidulans penicillin biosynthesis and penicillin biosynthesis genes acvA and ipnA by glucose.
J Bacteriol. 1992 Jun;174(11):3789-99
PMID: 1592830
-
Secondary metabolism, inventive evolution and biochemical diversity--a review.
Gene. 1992 Jun 15;115(1-2):135-40
PMID: 1612428
-
Carbon catabolite repression can account for the temporal pattern of expression of a penicillin biosynthetic gene in Aspergillus nidulans.
Mol Microbiol. 1992 Jun;6(11):1457-65
PMID: 1625576
-
The Aspergillus nidulans npeA locus consists of three contiguous genes required for penicillin biosynthesis.
EMBO J. 1990 Jan;9(1):279-87
PMID: 2403928
-
Either of two functionally redundant sensor proteins, NarX and NarQ, is sufficient for nitrate regulation in Escherichia coli K-12.
Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8419-23
PMID: 1528845
-
Penicillin and cephalosporin biosynthetic genes: structure, organization, regulation, and evolution.
Annu Rev Microbiol. 1992;46:461-95
PMID: 1444264
-
L-lysine repression of penicillin biosynthesis and the expression of penicillin biosynthesis genes acvA and ipnA in Aspergillus nidulans.
FEMS Microbiol Lett. 1992 Nov 1;77(1-3):123-7
PMID: 1369977
-
pH regulation is a major determinant in expression of a fungal penicillin biosynthetic gene.
EMBO J. 1993 Oct;12(10):3947-56
PMID: 8404862
-
Analysis of the regulation of penicillin biosynthesis in Aspergillus nidulans by targeted disruption of the acvA gene.
Mol Gen Genet. 1994 Jan;242(1):57-64
PMID: 8277946
-
Catabolism of lysine in Penicillium chrysogenum leads to formation of 2-aminoadipic acid, a precursor of penicillin biosynthesis.
Appl Environ Microbiol. 1994 Jun;60(6):1705-10
PMID: 8031073
-
Molecular characterization of aflR, a regulatory locus for aflatoxin biosynthesis.
Appl Environ Microbiol. 1994 Jul;60(7):2408-14
PMID: 8074521
-
Expression studies with the bidirectional pcbAB-pcbC promoter region from Acremonium chrysogenum using reporter gene fusions.
Appl Microbiol Biotechnol. 1994 Oct;42(1):57-66
PMID: 7765820
-
The genetics of Aspergillus nidulans.
Adv Genet. 1953;5:141-238
PMID: 13040135
-
GENETIC ANALYSIS OF THE PHOSPHATASES IN ASPERGILLUS NIDULANS.
Genet Res. 1965 Feb;6:13-26
PMID: 14301537
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Beta-galactosidase activity and lactose utilization in Aspergillus nidulans.
J Gen Microbiol. 1973 Aug;77(2):417-86
PMID: 4584063
-
Nuclear and extranuclear inheritance of oligomycin resistance in Aspergillus nidulans.
Mol Gen Genet. 1973 Nov 12;126(3):201-16
PMID: 4593756
-
Carbon catabolite repression in Aspergillos nidulans.
Eur J Biochem. 1975 Feb 21;51(2):573-7
PMID: 168071
-
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
Anal Biochem. 1976 May 7;72:248-54
PMID: 942051
-
Genetics of biosynthesis and overproduction of penicillin.
Sci Prog. 1976 Winter;63(252):547-73
PMID: 823642
-
Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4
PMID: 388439
-
A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
Anal Biochem. 1983 Jul 1;132(1):6-13
PMID: 6312838
-
Cloning an Aspergillus nidulans developmental gene by transformation.
EMBO J. 1985 May;4(5):1307-11
PMID: 3891328
-
Regulation of gene expression by pH of the growth medium in Aspergillus nidulans.
Mol Gen Genet. 1986 May;203(2):346-53
PMID: 3016485
-
A system for the analysis of expression signals in Aspergillus.
Gene. 1986;48(2-3):211-7
PMID: 3549463
-
The frdR gene of Escherichia coli globally regulates several operons involved in anaerobic growth in response to nitrate.
J Bacteriol. 1988 Feb;170(2):623-9
PMID: 3276662
-
Transformation of Penicillium chrysogenum using dominant selection markers and expression of an Escherichia coli lacZ fusion gene.
Gene. 1988;62(1):127-34
PMID: 3131191
-
Bacillus subtilis phenylalanyl-tRNA synthetase genes: cloning and expression in Escherichia coli and B. subtilis.
J Bacteriol. 1989 Feb;171(2):1228-32
PMID: 2492510
-
Regulatory genes in Aspergillus nidulans.
Trends Genet. 1989 Jan;5(1):14-9
PMID: 2652389
-
Cloning and characterization of beta-lactam biosynthetic genes.
Mol Microbiol. 1989 May;3(5):689-95
PMID: 2668696
-
pH regulation of penicillin production in Aspergillus nidulans.
FEMS Microbiol Lett. 1991 Jan 15;61(2-3):209-12
PMID: 2037230