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The specific transport system for lysine is fully inhibited by ammonium in Penicillium chrysogenum: An ammonium-insensitive system allows uptake in carbon-starved cells

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Abstract

The regulation exerted by ammonium and other nitrogen sources on amino acid utilization was studied in swollen spores of Penicillium chrysogenum. Ammonium prevented the L-lysine, L-arginine and L-ornithine utilization by P. chrysogenum swollen spores seeded in complete media, but not in carbon-deficient media. Transport of L-[14C]lysine into spores incubated in presence of carbon and nitrogen sources was fully inhibited by ammonium ions (35 mM). However, in carbon-derepressed conditions (growth in absence of sugars, with amino acids as the sole carbon source) L-[14C]lysine transport was only partially inhibited. Competition experiments showed that L-lysine (1 mM) inhibits the utilization of L-arginine, and vice versa, L-arginine inhibits the L-lysine uptake. High concentrations of L-ornithine (100 mM) prevented the L-lysine and L-arginine utilization in P. chrysogenum swollen spores. In summary, ammonium seems to prevent the utilization of basic amino acids in P. chrysogenum spores by inhibiting the transport of these amino acids through their specific transport system(s), but not through the general amino acid transport system that is operative under carbon-derepression conditions.

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References

  • Bañuelos O, Casqueiro J, Fierro F, Hijarrubia MJ, Gutiérrez S & Martín JF (1999) Characterization and lysine control expression of the lys1 gene of Penicillium chrysogenum encoding homocitrate synthase. Gene 226: 51–59

    Google Scholar 

  • Beckerich JM & Heslot H (1978) Physiology of lysine permeases in Saccharomycopsis lipolytica. J. Bacteriol. 113: 492–498

    Google Scholar 

  • Benko PV, Wood TC & Segel IH (1967) Specificity and regulation of methionine transport in filamentous fungi. Arch. Biochem. Biophys. 122: 783–804

    Google Scholar 

  • Benko PV, Wood TC & Segel IH (1969) Multiplicity and regulation of amino acid transport in Penicillium chrysogenum. Arch. Biochem. Biophys. 129: 498–508

    Google Scholar 

  • Casqueiro J, Gutiérrez S, Bañuelos O, Fierro F, Velasco J & Martín JF (1998) Characterization of the lys2 gene of Penicillium chrysogenum encoding α-aminoadipic acid reductase. Mol. Gen. Genet. 259: 549–556

    Google Scholar 

  • Casqueiro J, Gutiérrez S, Bañuelos O, Hijarrubia MJ & Martín JF (1999) Gene targeting in Penicillium chrysogenum: disruption of the lys2 gene leads to penicillin overproduction. J. Bacteriol. 181: 1181–1188

    Google Scholar 

  • Díez B, Gutiérrez S, Barredo JL, van Solingen P, van deer Voort LHM & Martín JF (1990) The cluster of penicillin biosynthetic genes. Identification and characterization of the pcbAB gene encoding the α-aminoadipyl-cysteinyl-valine synthetase and linkage to the pcbC and penDE genes. J. Biol. Chem. 265: 16358–16365

    Google Scholar 

  • Esmahan C, Alvarez E, Montenegro E & Martín JF (1994) Catabolism of lysine in Penicillium chrysogenum leads to formation of 2-aminoadipic acid, a precursor of penicillin biosynthesis. Appl. Environm. Microbiol. 60: 1705–1710

    Google Scholar 

  • Fierro F, Barredo JL, Díez B, Gutiérrez S, Fernández FJ & Martín JF (1995) The penicillin gene cluster is amplified in tandem repeats linked by conserved hexanucleotide sequences. Proc. Natl. Acad. Sci. USA 92: 6200–6204

    Google Scholar 

  • Greasham RL & Moat AG (1973) Amino acid transport in polyaromatic amino acid auxotroph of Saccharomyces cerevisiae. J. Bacteriol. 115: 975–981

    Google Scholar 

  • Grenson M, Hou C & Crabeel M (1970) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae: IV. Evidence for a general amino acid permease. J. Bacteriol. 103: 770–777

    Google Scholar 

  • Hillenga DJ, Versantvoort JM, Driessen AJM & Konings WN (1996) Basic amino acid transport in plasma membrane vesicles of Penicillium chrysogenum. J. Bacteriol. 178: 3991–3995

    Google Scholar 

  • Holliday R (1956) A new method for the identification of biochemical mutants of microorganism. Nature 178: 987

    Google Scholar 

  • Hönlinger C & Kubicek CP (1989) Regulation of δ-(-L-α-aminoadipyl)-L-cysteinyl-D-valine and isopenicillin N biosynthesis in Penicillium chrysogenum by the α-aminoadipate pool size. FEMS Microbiol. Lett. 65: 71–76

    Google Scholar 

  • Horák J (1986) Amino acid transport in eucaryotic microorganism. Biochim. Biophys. Acta 864: 223–256

    Google Scholar 

  • Hunter DR & Segel IH (1971) Acidic and basic amino acid transport systems of Penicillium chrysogenum. Arch. Biochem. Biophys. 144: 168–183

    Google Scholar 

  • Hunter DR & Segel IH (1973a) Control of the general amino acid permease of Penicillium chrysogenum by transinhibition and turnover. Arch. Biochem. Biophys. 154: 387–399

    Google Scholar 

  • Hunter DR & Segel IH (1973b) Effect of weak acids on amino acid transport by Penicillium chrysogenum: evidence for a proton or charge gradient as the driving force. J. Bacteriol. 113: 1184–1192

    Google Scholar 

  • Hunter DR, Norberg CL & Segel IH (1973) Effect of cycloheximide on L-leucine transport by Penicillium chrysogenum: involvement of calcium. J. Bacteriol. 114: 956–960

    Google Scholar 

  • Jaklitsch WM. & Kubicek CP (1990) Homocitrate synthase from Penicillium chrysogenum: localization, purification of the cytosolic isoenzyme, and sensitivity to lysine. Biochem. J. 269: 247–253

    Google Scholar 

  • López-Nieto MH, Ramos FR, Luengo JM & Martin JF (1985) Characterization of the biosynthesis in vivo of α-aminoadipyl-cysteinyl-valine in Penicillium chrysogenum. Appl. Microbiol. Biotechnol. 22: 343–351

    Google Scholar 

  • Lu Y, Mach RL, Affenzeller K & Kubicek P (1992) Regulation of α-aminoadipate reductase from Penicillium chrysogenum in relation to the flux from α-aminoadipate into penicillin biosynthesis. Can. J. Microbiol. 38: 758–763

    Google Scholar 

  • Luengo JM, Revilla G, LópezMJ, Villanueva JR & Martin JF (1980) Inhibition and repression of homocitrate synthase by lysine in Penicillium chrysogenum. J. Bacteriol. 144: 869–876

    Google Scholar 

  • Martín JF (1998) New aspects of genes and enzymes for β-lactam antibiotic biosynthesis. Appl. Microbiol. Biotechnol. 50: 1–15

    Google Scholar 

  • Martín JF, Liras P & Villanueva JR (1974) Changes in composition of conidia of Penicillium notatum during germination. Arch. Microbiol. 97: 39–50

    Google Scholar 

  • Martín JF, Gutiérrez S & Demain AL (1997) β-Lactams. In: Anke, T. (Ed) Fungal Biotechnology (pp 91–127). Chapman & Hall, Weinheim

    Google Scholar 

  • Morrison CE & Lichstein HC (1976) Regulation of lysine transport by feedback inhibition in Saccharomyces cerevisiae. J. Bacteriol. 125: 864–871

    Google Scholar 

  • Pateman JA, Kinghorn JR & Dunn E (1974) Regulatory aspects of L-glutamate transport in Aspergillus nidulans. J. Bacteriol. 119: 534–542

    Google Scholar 

  • Piotrowska M, Stepien PP, Bartnik E & Zakrzewska E (1976) Basic and neutral amino acid transport in Aspergillus nidulans. J.Gen. Microbiol. 92: 89–96

    Google Scholar 

  • Robinson JH, Anthony C & Drabble WT (1973) Regulation of the acidic amino acid permease of Aspergillus nidulans. J. Gen. Microbiol. 79: 65–80

    Google Scholar 

  • Roos W (1989) Kinetics properties, nutrient-dependent regulation and energy coupling of amino acid transport systems in Penicillium cyclopium. Biochim. Biophys. Acta 978: 119–133

    Google Scholar 

  • Skye GE & Segel IH (1970) Independent regulation of cysteine and cystine transport in Penicillium chrysogenum. Arch. Biochem. Biophys. 138: 306–318

    Google Scholar 

  • Tisdale JH & DeDusk AG (1970) Developmental regulation of amino acid transport in Neurospora crassa. J. Bacteriol. 104: 689–697

    Google Scholar 

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Authors and Affiliations

  1. Area of Microbiology, Faculty of Biology, University of León, 24071, León

    Oscar Bañuelos, Santiago Gutiérrez, Jorge Riaño & Juan F. Martín

  2. Science Park of León, Institute of Biotechnology INBIOTEC, Avda. del Real, no. 1, 24006, León, Spain

    Javier Casqueiro, Santiago Gutiérrez & Jorge Riaño

Authors
  1. Oscar Bañuelos
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  2. Javier Casqueiro
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  3. Santiago Gutiérrez
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  4. Jorge Riaño
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  5. Juan F. Martín
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Correspondence to Juan F. Martín.

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Bañuelos, O., Casqueiro, J., Gutiérrez, S. et al. The specific transport system for lysine is fully inhibited by ammonium in Penicillium chrysogenum: An ammonium-insensitive system allows uptake in carbon-starved cells. Antonie Van Leeuwenhoek 77, 91–100 (2000). https://doi.org/10.1023/A:1002427916923

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