Compartmentalization in penicillin G biosynthesis by Penicillium chrysogenum PQ-96

• Autorzy: Kurzatkowski W. , Staniszewska M. , Bondaryk M. , Gebska-Kuczerowska A.
• Języki publikacji: EN

Abstrakty

EN

The arrangement of organelles in the sub-apical productive non-growing vacuolated hyphal cells of the high- and the low-penicillin-producing strains Penicillium chrysogenum was compared using transmission electron microscopy. In the productive cells of the high-yielding strain the endoplasmic reticulum and the polyribosomes with associated peroxisomes are frequently arranged at the periphery of the cytoplasm and around the vacuoles. At the high activity of penicillin G biosynthesis the immuno-label of the cytosolic isopenicillin N synthase is concentrated at the polyribosomes arranged in the peripheral cytoplasm and along the tonoplast as well as around the peroxisomes. On the basis of the obtained results the compartmentalization of the pathway of penicillin G biosymthesis is discussed. The obtained results support the phenylacetic acid detoxification hypothesis of penicillin G biosynthesis.

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2014
• Tom: 63
• Numer: 4
• Opis fizyczny: p.399-408,fig.,ref.

Twórcy

autor

Kurzatkowski W.

• Independent Laboratory of Streptomyces and Fungi Imperfecti, National Institute of Public Health-National Institute of Hygiene, Warsaw, Poland

autor

Staniszewska M.

• Independent Laboratory of Streptomyces and Fungi Imperfecti, National Institute of Public Health-National Institute of Hygiene, Warsaw, Poland

autor

Bondaryk M.

• Independent Laboratory of Streptomyces and Fungi Imperfecti, National Institute of Public Health-National Institute of Hygiene, Warsaw, Poland

autor

Gebska-Kuczerowska A.

• Independent Laboratory of Streptomyces and Fungi Imperfecti, National Institute of Public Health-National Institute of Hygiene, Warsaw, Poland

Bibliografia

• Antonenkov V.D. and J.K. Hiltunen. 2012. Transfer of metabolites across the peroxisomal membrane. Biochim. Biophys. Acta 1822: 1374–1386.
• Bartoszewska M., J.A. Kiel, R.A. Bovenberg, M. Veenhuis and I.J. van der Klei. 2011a. Autophagy deficiency promotes β-lactam production in Penicillium chrysogenum. Appl. Environ. Microbiol. 77: 1413–1422.
• Bartoszewska M., Ł. Opaliński, M. Veenhuis and I.J. van der Klei. 2011b. The significance of peroxisomes in secondary metabolite biosynthesis in filamentous fungi. Biotechnol. Lett. 33: 1921–1931.
• Brakhage A.A., P. Spröte, Q. Al-Abdallah, A. Gehrke, K. Plaftner and A. Tüncher. 2004. Regulation of penicillin biosynthesis in filamentous fungi. Adv. Biochem. Eng. Biotechnol. 88: 45–90.
• Evers M.E., H. Trip, M. A. van den Berg, R.A. Bovenberg andA.J. Driessen. 2004. Compartmentalization and transport in β-lactam antibiotics biosynthesis. Adv. Biochem. Eng. Biotechnol. 88: 111–135.
• Garcia-Estrada C., I. Vaca, F. Fierro, K. Sjollema, M. Veenhuis and J.F. Martin. 2008a. The unprocessed preprotein from IATC103S of the isopenicillin N acyltransferase is transported inside peroxisomes and regulates its self-processing. Fung. Genet. Biol. 45: 1043–1052.
• Garcίa-Estrada C., I. Vaca and M. Lamas-Maceiras. 2008b. In vivo transport of the intermediates of the penicillin biosynthetic pathway in tailored strains of Penicillium chrysogenum. Appl. Microbiol. 76: 169–182.
• Hillenga D.J., H.J. Versantvoort, S. van der Molen, A.J. Driessen and W.N. Konings. 1995. Penicillium chrysogenum takes up the penicillin G precursor phenylacetic acid by passive diffusion. Appl. Environ. Microbiol. 61: 2589–2595.
• Hoepfner D., D. Schildknegt, I. Braakman, P. Philippsen andH.F. Tabak. 2005. Contribution of the endoplasmic reticulum to peroxisome formation. Cell. 122: 85–95.
• Jourdain I., D. Sontam, C. Johnson, C. Dillies and J.S. Hyams. 2008. Dynamin-dependent biogenesis cell cycle regulation and mitochondrial association of peroxisomes in fission yeast. Traffic 9: 353–365.
• Keller N.P., G. Turner and J.W. Bennett. 2005. Fungal secondary metabolism-from biochemistry to genomics. Nat. Rev. Microbiol. 3: 937–947.
• Kiel J.A., M.A. van den Berg, F. Fusetti, B. Poolman, R.A. Bovenberg, M. Veenhuis and I.J. van der Klei. 2009. Matching the proteome to the genome: the microbody of penicillin-producing Penicillium chrysogenum cells. Funct. Integr. Genomics 9: 167–184.
• Kiel J.A., I.J. van der Klei, M.A. van den Berg, R.A. Bovenberg and M. Veenhuis. 2005. Overproduction of a single protein, Pc-Pex11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal. Genet. Biol. 42: 154–164.
• Koetsier M.J., P.A. Jekel, M.A. van den Berg, R.A. Bovenberg and D.B. Jenssen. 2009. Characterization of a phenylacetate – CoA ligase from Penicillium chrysogenum. Biochem. J. 417: 467–476.
• Kurzątkowski W., H. Palissa, H. Van Liempt, H. von Döhren,H. Kleinkauf, W.P. Wolf and W. Kuryłowicz. 1991. Localization of isopenicillin N synthase in Penicillium chrysogenum PQ-96. Appl. Microbiol. Biotechnol. 35: 517–520.
• Lendenfeld T., D. Ghali, M. Wolschek, E.M. Kubicek-Pranz and C.P. Kubicek. 1993. Subcellular compartmentation of penicillin biosynthesis in Penicillium chrysogenum – the amino acids are precursors derived from the vacuole. J. Biol. Chem. 268: 665–671.
• Martin J-F., R.V. Ullán and C. Garcia-Estrada. 2010. Regulation and compartmentalization of β-lactam biosynthesis. Microb. Biotechnol. 3: 285–299.
• Martin J-F., Ullán R.V. and C. Garcia-Estrada. 2012. Role of peroxisomes in the biosynthesis and secretion of β-lactams and other secondary metabolites. J. Ind. Microbiol. Biotechnol. 39: 367–382.
• Meijer W.H., L. Gidijala, S. Fekken, J.A. Kiel, M.A. van den Berg, R. Lascaris, A.L. Roal, R.A. Bovenberg and I.J. van der Klei. 2010. Peroxisomes are required for efficient penicillin biosynthesis in Penicillium chrysogenum. Appl. Environ. Microbiol. 76: 5702–5709.
• Motley A.M. and E.H. Hettema. 2007. Yeast peroxisomes multiply by growth and division. J. Cell. Biol. 178: 399–410.
• Motley AM, G.P. Ward and E.H. Hettema. 2008. Dnm1p-dependent peroxisome fission requires Caf4p, Mdv1p and Fis1p. J. Cell. Sci. 121: 1633–1640.
• Müller W.H., J. Essers, B.M. Humbel and A.J. Verkleij. 1995. Enrichment of Penicillium chrysogenum microbodies by isopycnic centrifugation in nycodenz as visualized with immuno-electron microscopy. Biochem. Biophys. Acta 1245: 215–220.
• Nagotu S., M. Veenhuis and I.J. van der Klei. 2010. Divide et impera: The dictum of peroxisomes. Traffic 11: 175–184.
• Nuttall J.M., A. Motley and E.H. Hettema. 2011. Peroxisome biogenesis recent advances. Curr. Opin. Cell. Biol. 23: 421–426.
• Opaliński Ł, J.A. Kiel, T.G. Homan, M. Veenhuis and I.J. van der Klei. 2010. Penicillium chrysogenum Pex14/17p – a novel component of the peroxisomal membrane that is important for penicillin production. FEBS J. 277: 3203–3218.
• Opaliński Ł., M. Bartoszewska, S. Fekken, H. Liu, R. de Boer,I. van der Klei, M. Veenhuis and J.A. Kiel. 2012. De Novo peroxisome biogenesis in Penicillium chrysogenum is not dependent on the Pex11 family members or Pex16. PLoS ONE 7: e35490, DOI: 10.1371/journal.pone.0035490.
• Paul G.C. and C.R. Thomas. 1996. A structured model for hyphal differentiation and penicillin production using Penicillium chrysogenum. Biotechnol. Bioeng. 51: 558–572.
• Perry R.J., F.D. Mast and R.A. Rachubiński. 2009. Endoplasmic reticulum-associated secretory proteins Sec20p, Sec39p and Dsl1p are involved in peroxisome biogenesis. Eukaryot. Cell. 8: 830–843.
• Tam Y.Y., A. Fagarasanu, M. Fagarasanu and R.A. Rachubiński. 2005. Pex3p initiates the formation of a preperoxisomal compartment from a subdomain of the endoplasmic reticulum in Saccharomyces cerevisiae. J. Biol. Chem. 280: 34933–34939.
• Theilgaard H.B., K.N. Kristiansen, C.M. Henriksen and J. Nielsen. 1997. Purification and characterization of δ-(L-α-aminoadipyl)-L-cysteinyl-D-valine synthetase from Penicillium chrysogenum. Biochem. J. 327: 185–191.
• Thykaer J. and J. Nielsen. 2003. Metabolic engineering of β-lactam production. Metab. Eng. 5: 56–69.
• van de Kamp M., A.J. Driessen and W.N Konings. 1999. Compartmentalization and transport in β-lactam antibiotic biosynthesis by filamentous fungi. Antonie van Leeuwenhoek 75: 41–78.
• van den Berg M.A., R. Albang, K. Albermann, J.H. Badger,J-M. Daran, A.J. Driessen, C. Garcia-Estrada, N.D. Fedorova, D.M. Harris, W.H. Heijne and others. 2008. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26: 1161–1168.
• van der Lende T.R., M. van de Kamp, M. van den Berg, K. Sjollema, R.A. Bovenberg, M. Veenhuis, W.N. Konings and A.J. Driessen. 2002a. δ-(L-α-Aminoadipyl)-L-cysteinyl-D-valine synthetase, that mediates the first committed step in penicillin biosynthesis, is a cytosolic enzyme. Fungal. Genet. Biol. 37: 49–55.
• van der Lende T.R., P. Breeuwer, T. Abee, W.N. Konings and A.J. Driessen. 2002b. Assessment of the microbody luminal pH in the filamentous fungus Penicillium chrysogenum. Biochim. Biophys. Acta 1589: 104–111.
• Weber S.S., R.A. Bovenberg and A.J. Driessen. 2012a. Biosynthetic concepts for the production of β-Lactam antibiotics in Penicillium chrysogenum. Biotechnol. J. 7: 225–236.
• Weber S.S., F. Polli, R. Boer, R.A. Bovenberg and A.J. Driessen. 2012b. Increased penicillin production in Penicillium chrysogenum strains via balanced overexpression of isopenicillin N acyltransferase. Appl. Envitron. Microbiol. 78: 7107–7113.