Peroxisomes contribute to biosynthesis of extracellular glycolipids in fungi

Molecular Microbiology

Volumn 93, Issue 1, 2014, Pages 24-36

  Freitag, Johannes ^a,b   Ast, Julia ^a   Linne, Uwe ^a   Stehlik, Thorsten ^a   Martorana, Domenica ^a   Bölker, Michael ^a   Sandrock, Björn ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b SENCKENBERG DEUTSCHES ENTOMOLOGISCHES INSTITUT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; FATTY ACID; GLYCOLIPID; MAC1 PROTEIN; MAC2 PROTEIN; MANNOSYLERYTHRITOL LIPID; UNCLASSIFIED DRUG; USTILAGIC ACID; FUNGAL PROTEIN;

ACYLATION; ARTICLE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME STRUCTURE; FATTY ACID OXIDATION; LIPID DEGRADATION; LIPOGENESIS; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN TARGETING; TYPE 1 PEROXISOMAL TARGETING SIGNAL; USTILAGO MAYDIS; CHEMISTRY; CYTOSOL; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; USTILAGO;

FUNGI; USTILAGO MAYDIS;

ACETYLTRANSFERASES; ACYLATION; AMINO ACID MOTIFS; BIOSYNTHETIC PATHWAYS; CYTOSOL; FATTY ACIDS; FUNGAL PROTEINS; GLYCOLIPIDS; MUTATION; PEROXISOMES; USTILAGO;

EID: 84903483787     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12642     Document Type: Article

References (69)

1. Abràmoff, M.D., Hospitals, I., Magalhães, P.J., and Abràmoff, M. (2004) Image processing with ImageJ. Biophotonics Int 11: 36-42.
2. Bartoszewska, M., Opalinski, L., Veenhuis, M., and van der Klei, I.J. (2011) The significance of peroxisomes in secondary metabolite biosynthesis in filamentous fungi. Biotechnol Lett 33: 1921-1931.
3. Böhmer, C., Böhmer, M., Bölker, M., and Sandrock, B. (2008) Cdc42 and the Ste20-like kinase Don3 act independently in triggering cytokinesis in Ustilago maydis. J Cell Sci 121: 143-148.
4. Bölker, M., Basse, C.W., and Schirawski, J. (2008) Ustilago maydis secondary metabolism - from genomics to biochemistry. Fungal Genet Biol 45: S88-S93.
5. Brachmann, A., König, J., Julius, C., and Feldbrügge, M. (2004) A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272: 216-226.
6. Brocard, C., and Hartig, A. (2006) Peroxisome targeting signal 1: is it really a simple tripeptide? Biochim Biophys Acta 1763: 1565-1573.
7. Brocard, C., Kragler, F., Simon, M.M., Schuster, T., and Hartig, A. (1994) The Tetratricopeptide repeat domain of the PAS10 protein of Saccharomyces cerevisiae is essential for binding the peroxisomal targeting signal-SKL. Biochem Biophys Res Commun 204: 1016-1022.
8. Broomfield, P.L.E., and Hargreaves, J.A. (1992) A single amino-acid change in the iron-sulphur protein subunit of succinate dehydrogenase confers resistance to carboxin in Ustilago maydis. Curr Genet 22: 117-121.
9. Chanda, A., Roze, L.V., Pastor, A., Frame, M.K., and Linz, J.E. (2009a) Purification of a vesicle-vacuole fraction functionally linked to aflatoxin synthesis in Aspergillus parasiticus. J Microbiol Methods 78: 28-33.
10. Chanda, A., Roze, L.V., Kang, S., Artymovich, K.A., Hicks, G.R., Raikhel, N.V., etal. (2009b) A key role for vesicles in fungal secondary metabolism. Proc Natl Acad Sci USA 106: 19533-19538.
11. de Duve, C., and Baudhuin, P. (1966) Peroxisomes (microbodies and related particles). Physiol Rev 46: 323-357.
12. Frautz, B., Lang, S., and Wagner, F. (1986) Formation of cellobiose lipids by growing and resting cells of Ustilago maydis. Biotechnol Lett 8: 757-762.
13. Freitag, J., Lanver, D., Böhmer, C., Schink, K.O., Bölker, M., and Sandrock, B. (2011) Septation of infectious hyphae is critical for appressoria formation and virulence in the smut fungus Ustilago maydis. PLoS Pathog 7: 5e1002044.
14. Freitag, J., Ast, J., and Bölker, M. (2012) Cryptic peroxisomal targeting via alternative splicing and stop codon read-through in fungi. Nature 485: 522-525.
15. Gabaldón, T. (2010) Peroxisome diversity and evolution. Philos Trans R Soc Lond B Biol Sci 365: 765-773.
16. Gietz, D.R., and Woods, R.A. (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350: 87-96.
17. Gould, S.J., Keller, G.A., Hosken, N., Wilkinson, J., and Subramani, S. (1989) A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol 108: 1657-1664.
18. Gould, S.J., Keller, G.A., Schneider, M., Howell, S.H., Garrard, L.J., Goodman, J.M., etal. (1990) Peroxisomal protein import is conserved between yeast, plants, insects and mammals. EMBO J 9: 85-90.
19. Gründlinger, M., Yasmin, S., Lechner, B.E., Geley, S., Schrettl, M., Hynes, M., and Haas, H. (2013) Fungal siderophore biosynthesis is partially localized in peroxisomes. Mol Microbiol 88: 862-875.
20. Haskins, R.H., and Thorn, J.A. (1951) Biochemistry of the ustilaginales: VII. Antibiotic activity of ustilagic acid. Can J Bot 29: 585-592.
21. Haskins, R.H., Thorn, J.A., and Boothroyd, B. (1955) Biochemistry of the Ustilaginales: XI. Metabolic products of Ustilago zeae in submerged culture. Can J Microbiol 1: 749-756.
22. Hewald, S., Josephs, K., and Bölker, M. (2005) Genetic analysis of biosurfactant production in Ustilago maydis. Appl Environ Microbiol 71: 3033-3040.
23. Hewald, S., Linne, U., Scherer, M., Marahiel, M.A., Kämper, J., and Bölker, M. (2006) Identification of a gene cluster for biosynthesis of mannosylerythritol lipids in the basidiomycetous fungus Ustilago maydis. Appl Environ Microbiol 72: 5469-5477.
24. Hoffman, C.S., and Winston, F. (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformaion of Escherichia coli. Gene 57: 267-272.
25. Hong, S.-Y., and Linz, J.E. (2009) Functional expression and sub-cellular localization of the early aflatoxin pathway enzyme Nor-1 in Aspergillus parasiticus. Mycol Res 113: 591-601.
26. Hynes, M.J., Murray, S.L., Khew, G.S., and Davis, M.A. (2008) Genetic analysis of the role of peroxisomes in the utilization of acetate and fatty acids in Aspergillus nidulans. Genetics 178: 1355-1369.
27. Idnurm, A., Giles, S.S., Perfect, J.R., and Heitman, J. (2007) Peroxisome function regulates growth on glucose in the basidiomycete fungus Cryptococcus neoformans. Eukaryot Cell 6: 60-72.
28. Imazaki, A., Tanaka, A., Harimoto, Y., Yamamoto, M., Akimitsu, K., Park, P., and Tsuge, T. (2010) Contribution of peroxisomes to secondary metabolism and pathogenicity in the fungal plant pathogen Alternaria alternata. Eukaryot Cell 9: 682-694.
29. Jedd, G., and Chua, N.H. (2000) A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2: 226-231.
30. van de Kamp, M., Driessen, A.J.M., and Konings, W.N. (1999) Compartmentalization and transport in β-lactam antibiotic biosynthesis by filamentous fungi. Antonie Van Leeuwenhoek 75: 41-78.
31. Kämper, J. (2004) A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol Genet Genomics 271: 103-110.
32. Keller, N.P., Turner, G., and Bennett, J.W. (2005) Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol 3: 937-947.
33. Kitamoto, D., Yanagishita, H., Haraya, K., and Kitamoto, H.K. (1998) Contribution of a chain-shortening pathway to the biosynthesis of the fatty acids of mannosylerythritol lipid (biosurfactant) in the yeast Candida antarctica: effect of β-oxidation inhibitors on biosurfactant synthesis. Biotechnol Lett 20: 813-818.
34. Kitamoto, D., Isoda, H., and Nakahara, T. (2002) Functions and potential applications of glycolipid biosurfactants - from energy-saving materials to gene delivery carriers. J Biosci Bioeng 94: 187-201.
35. Klose, J., and Kronstad, J.W. (2006) The multifunctional β-oxidation enzyme is required for full symptom development by the biotrophic maize pathogen Ustilago maydis. Eukaryot Cell 5: 2047-2061.
36. Kretschmer, M., Klose, J., and Kronstad, J.W. (2012) Defects in mitochondrial and peroxisomal β-oxidation influence virulence in the maize pathogen Ustilago maydis. Eukaryot Cell 11: 1055-1066.
37. Kurylowicz, W., Kurzatkowski, W., and Kurzatkowski, J. (1987) Biosynthesis of benzylpenicillin by Penicillium chrysogenum and its Golgi apparatus. Arch Immunol Ther Exp (Warsz) 35: 699-724.
38. Kurz, M., Eder, C., Isert, D., Li, Z., Paulus, E.F., Schiell, M., etal. (2003) Ustilipids, acylated beta-D-mannopyranosyl D-erythritols from Ustilago maydis and Geotrichum candidum. J Antibiot (Tokyo) 56: 91-101.
39. Lazarow, P.B. (2006) The import receptor Pex7p and the PTS2 targeting sequence. Biochim Biophys Acta Mol Cell Res 1763: 1599-1604.
40. Lee, L.-W., Chiou, C.-H., Klomparens, K.L., Cary, J.W., and Linz, J.E. (2004) Subcellular localization of aflatoxin biosynthetic enzymes Nor-1, Ver-1, and OmtA in time-dependent fractionated colonies of Aspergillus parasiticus. Arch Microbiol 181: 204-214.
41. van der Leij, I., Franse, M.M., Elgersma, Y., Distel, B., and Tabak, H.F. (1993) PAS10 is a tetratricopeptide-repeat protein that is essential for the import of most matrix proteins into peroxisomes of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 90: 11782-11786.
42. Lendenfeld, T., Ghali, D., Wolschek, M., Kubicek-Pranz, E.M., and Kubicek, C.P. (1993) Subcellular compartmentation of penicillin biosynthesis in Penicillium chrysogenum. The amino acid precursors are derived from the vacuole. J Biol Chem 268: 665-671.
43. Lingner, T., Kataya, A.R., Antonicelli, G.E., Benichou, A., Nilssen, K., Chen, X.-Y., etal. (2011) Identification of novel plant peroxisomal targeting signals by a combination of machine learning methods and in vivo subcellular targeting analyses. Plant Cell 23: 1556-1572.
44. Maggio-Hall, L.A., Wilson, R.A., and Keller, N.P. (2005) Fundamental contribution of β-oxidation to polyketide mycotoxin production in planta. Mol Plant Microbe Interact 18: 783-793.
45. Magliano, P., Flipphi, M., Arpat, B.A., Delessert, S., and Poirier, Y. (2011) Contributions of the peroxisome and β-oxidation cycle to biotin synthesis in fungi. J Biol Chem 286: 42133-42140.
46. Marchant, R., and Banat, I. (2012a) Biosurfactants: a sustainable replacement for chemical surfactants? Biotechnol Lett 34: 1597-1605.
47. Marchant, R., and Banat, I.M. (2012b) Microbial biosurfactants: challenges and opportunities for future exploitation. Trends Biotechnol 30: 558-565.
48. Marchesini, S., and Poirier, Y. (2003) Futile cycling of intermediates of fatty acid biosynthesis toward peroxisomal β-oxidation in Saccharomyces cerevisiae. J Biol Chem 278: 32596-32601.
49. Marzioch, M., Erdmann, R., Veenhuis, M., and Kunau, W.-H. (1994) PAS7 encodes a novel yeast member of the WD-40 protein family essential for import of 3-oxoacyl-CoA thiolase, a PTS2-containing protein, into peroxisomes. EMBO J 13: 4908-4918.
50. Mortimer, R.K., and Johnston, J.R. (1986) Genealogy of principal strains of the yeast genetic stock center. Genetics 113: 35-43.
51. Müller, W.H., der Krift, T.P., Krouwer, A.J., Wösten, H.A., van der Voort, L.H., Smaal, E.B., and Verkleij, A.J. (1991) Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum. EMBO J 3: 489-495.
52. Müller, W.H., Bovenberg, R.A.L., Groothuis, M.H., Kattevilder, F., Smaal, E.B., van der Voort, L.H., and Verkleij, A.J. (1992) Involvement of microbodies in penicillin biosynthesis. Biochim Biophys Acta 1116: 210-213.
53. Neuberger, G., Maurer-Stroh, S., Eisenhaber, B., Hartig, A., and Eisenhaber, F. (2003a) Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J Mol Biol 328: 567-579.
54. Neuberger, G., Maurer-Stroh, S., Eisenhaber, B., Hartig, A., and Eisenhaber, F. (2003b) Prediction of peroxisomal targeting signal 1 containing proteins from amino acid sequence. J Mol Biol 328: 581-592.
55. Opperdoes, F.R., and Borst, P. (1977) Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Lett 80: 360-364.
56. Poirier, Y., Antonenkov, V.D., Glumoff, T., and Hiltunen, J.K. (2006) Peroxisomal β-oxidation - a metabolic pathway with multiple functions. Biochim Biophys Acta 1763: 1413-1426.
57. Roze, L.V., Chanda, A., and Linz, J.E. (2011) Compartmentalization and molecular traffic in secondary metabolism: a new understanding of established cellular processes. Fungal Genet Biol 48: 35-48.
58. Rucktäschel, R., Girzalsky, W., and Erdmann, R. (2011) Protein import machineries of peroxisomes. Biochim Biophys Acta Biomembr 1808: 892-900.
59. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Schjerling, C.K., Hummel, R., Hansen, J.K., Børsting, C., Mikkelsen, J.M., Kristiansen, K., and Knudsen, J. (1996) Disruption of the gene encoding the acyl-CaA-binding protein (ACB1) perturbs acyl-CoA metabolism in Saccharomyces cerevisiae. J Biol Chem 271: 22514-22521.
61. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schäfer, W., Martin, T., etal. (1990) The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60: 295-306.
62. Spellig, T., Bottin, A., and Kahmann, R. (1996) Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol Gen Genet 252: 503-509.
63. Spröte, P., Brakhage, A.A., and Hynes, M.J. (2009) Contribution of peroxisomes to penicillin biosynthesis in Aspergillus nidulans. Eukaryot Cell 8: 421-423.
64. Srere, P.A. (1987) Complexes of sequential metabolic enzymes. Annu Rev Biochem 56: 89-124.
65. Tanabe, Y., Maruyama, J., Yamaoka, S., Yahagi, D., Matsuo, I., Tsutsumi, N., and Kitamoto, K. (2011) Peroxisomes are involved in biotin biosynthesis in Aspergillus and Arabidopsis. J Biol Chem 286: 30455-30461.
66. Teichmann, B., Linne, U., Hewald, S., Marahiel, M.A., and Bölker, M. (2007) A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Mol Microbiol 66: 525-533.
67. 2 zinc finger transcription factor Rua1. Appl Environ Microbiol 76: 2633-2640.
68. Teichmann, B., Labbé, C., Lefebvre, F., Bölker, M., Linne, U., and Bélanger, R.R. (2011) Identification of a biosynthesis gene cluster for flocculosin a cellobiose lipid produced by the biocontrol agent Pseudozyma flocculosa. Mol Microbiol 79: 1483-1495.
69. Winterberg, B., Uhlmann, S., Linne, U., Lessing, F., Marahiel, M.A., Eichhorn, H., etal. (2010) Elucidation of the complete ferrichrome A biosynthetic pathway in Ustilago maydis. Mol Microbiol 75: 1260-1271.