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Genetic instability of the short-living ascomycetous fungus Podospora anserina induced by prolonged submerged cultivation

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Abstract

Investigation of genetic variability of the short-living filamentous fungus Podospora anserina during its adaptation to conditions of prolonged submerged cultivation has been carried out for the first time. Cultivation of P. anserina under aeration (on a shaker) provides pronounced selective pressure, which makes it possible to obtain isolates with specific features, which are well adapted to cultivation in liquid media and have a life span several times exceeding that of the original strain. Static cultivation did not prevent the ageing of P. anserina. Repeated transfers in the shaker culture resulted in formation of mycelium deprived of the dark pigment melanin and actively producing carotenoids under illumination. The qualitative composition of P. anserina carotenoids was the same as in the closely-related species Neurospora crassa. The features obtained during the shaker cultivation (including changes in the colony morphology and decreased capacity for melanin synthesis) are inherited by their hybrids with the wild type strains, i.e., they resulted from the intragenomic rearrangements occurring during submerged cultivation of the fungus.

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References

  1. Burdon, J.J. and Silk, J., Sources and Patterns of Diversity in Plant-Pathogenic Fungi, Phytopathology, 1997, vol. 87, no. 7, pp. 664–669.

    Article  PubMed  CAS  Google Scholar 

  2. Chetverikova, E.P., The Problem of Stability of Organisms after Cryopreservation (Fungi as Example), Biofizika, 2009, vol. 54, no. 5, pp. 887–893 [Biophysics (Engl. Transl.), vol. 54, no. 5, pp. 626–630].

    PubMed  CAS  Google Scholar 

  3. Dunham, M.J., Badrane, H., Ferea, T., Adams, J., Brown, P.O., Rosenzweig, F., and Botstein, D., Characteristic Genome Rearrangements in Experimental Evolution of Saccharomyces cerevisiae, PNAS, 2002, vol. 99, no. 25, pp. 16144–16149.

    Article  PubMed  CAS  Google Scholar 

  4. Galagan, J.E., Henn, M.R., Ma, L.J., Cuomo, C.A., and Birren, B., Genomics of the Fungal Kingdom: Insights into Eukaryotic Biology, Genome Res., 2005, vol. 15, pp. 1620–1631.

    Article  PubMed  CAS  Google Scholar 

  5. Li, A., Begin, M., Kokurewicz, K., Bowden, C., and Horgen, P.A,. Inheritance of Strain Instability (Sectoring) in the Commercial Button Mushroom, Agaricus bisporus, Appl. Environ. Microbiol., 1994, vol. 60, no. 7, pp. 2384–2388.

    PubMed  CAS  Google Scholar 

  6. Cecília de Lima Fávaro, L., Luiz Araújo, W., Aparecida de Souza-Paccola, E., Lúcio Azevedo, J., Paccola-Meirelles, L.D. Colletotrichum sublineolum Genetic Instability Assessed by Mutants Resistant to Chlorate, Mycol. Res., 2007, vol. 111, no. 1, pp. 93–105.

    Article  PubMed  Google Scholar 

  7. van de Vondervoort, P.J., Poulsen, B.R., Ruijter, G.J., Schuleit, T., Visser, J., and Iversen, J.J., Isolation of a Fluffy Mutant of Aspergillus niger from Chemostat Culture and Its Potential Use as a Morphologically Stable Host for Protein Production, Biotechnol. Bioeng., 2004, vol. 86, no. 3, pp. 301–307.

    Article  PubMed  Google Scholar 

  8. Fursova, P.V., Mil’ko, E.S., Il’inykh, I.A., and Levich, A.P., Approaches to Monitoring the Community of Pseudomonas aeruginosa Variants: Experimental Data and Model Calculations, Biotekhnologiya, 2005, no. 1, pp. 73–82.

  9. Mil’ko, E.S., Kotova, I.B., and Netrusov, A.I., Protsess Dissotsiatsii u bakterii: Uchebnoe posobie (Phase Variation in Bacteria: A Textbook), Moscow: MAKS, 2007.

    Google Scholar 

  10. Çakar, Z.P., Metabolic and Evolutionary Engineering Research in Turkey and beyond, Biotechnol. J., 2009, vol. 4, pp. 992–1002.

    Article  PubMed  Google Scholar 

  11. Swift, R.J., Wiebe, M.G., Robson, G.D., and Trinci, A.P., Recombinant Glucoamylase Production by Aspergillus niger B1 in Chemostat and pH Auxostat Cultures, Fungal Genet. Biol., 1998, vol. 25, pp. 100–109.

    Article  PubMed  CAS  Google Scholar 

  12. Crecy, E., Jaronski, S., Lyons, B., Lyons, T.J., and Keyhani, N.O., Directed Evolution of a Filamentous Fungus for Thermotolerance, BMC Biotechnol., 2009, vol. 9, no. 74. http://www.biomedcentral.com/1472-6750/9/74.

  13. Coppin, E. and Silar, P., Identification of PaPKS1, a Polyketide Synthase Involved in Melanin Formation and Its Use as a Genetic Tool in Podospora anserina, Mycol. Res., 2007, vol. 111, no. 8, pp. 901–908.

    Article  CAS  Google Scholar 

  14. Espagne, E., Lespinet, O., Malagnac, F., Silva, C.D., Jaillon, O., Porcel, B.M., Couloux, A., Aury, J.M., Segurens, B., Poulain, J., Anthouard, V., Grossetete, S., Khalili, H., Coppin, E., Dequard-Chablat, M., Picard, M., Contamine, V., Arnaise, S., Bourdais, A., Berteaux-Lecellier, V., Gautheret, D., Vries, R.P., Battaglia, E., Coutinho, P.M., Danchin, E.G.J., Henrissat, B., Khoury, R.E.L., Sainsard-Chanet, A., Boivin, A., Pinan-Lucarre, B., Sellem, C.H., Debuchy, R., Wincker, P., Weissenbach, J., and Silar, P., The Genome Sequence of the Model Ascomycete Fungus Podospora anserina, Genome Biol., 2008, vol. 9, no. 5, pp. 1–22.

    Article  Google Scholar 

  15. Osiewacz, H.D., Aging and Mitochondrial Dysfunction in the Filamentous Fungus Podospora anserina, in Model Systems in Aging. Topics in Current Genetics, Nyström, T. and Osiewacz, H.D., Eds., Berlin: Springer, 2003, vol. 3, pp. 17–38.

    Google Scholar 

  16. Silar, P., Lalucque, H., and Vierny, C., Cell Degeneration in the Model System Podospora anserina, Biogerontology, 2001, vol. 2, pp. 1–17.

    Article  PubMed  CAS  Google Scholar 

  17. Osiewacz, H.D., Genes, Mitochondria and Aging in Filamentous Fungi, Ageing Res. Rev., 2002, vol. 1, pp. 425–442.

    Article  PubMed  CAS  Google Scholar 

  18. Sellem, C.H., Marsy, S., Boivin, A., Lemaire, C., and Sainsard-Chanet, A., A Mutation in the Gene Encoding Cytochrome c 1 Leads to a Decreased ROS Content and to a Long-Lived Phenotype in the Filamentous Fungus Podospora anserina, Fungal Genet. Biol., 2007, vol. 44, no. 7, pp. 648–658.

    Article  PubMed  CAS  Google Scholar 

  19. Turker, M.S. and Cummings, D.J., Podospora anserina Does Not Senesce when Serially Passaged in Liquid Culture, J. Bacteriol., 1987, vol. 169, no. 2, pp. 454–460.

    PubMed  CAS  Google Scholar 

  20. Rizet, G.. Les phénomênes de barrage chez Podospora anserina. I. Analyse génétique des barrages entre les souches S et s, Rev. Cytol. Biol. Veg., 1952, vol. 13, pp. 51–92.

    Google Scholar 

  21. Esser, K., The Genetics of Podospora anserina, in Handbook of Genetics, King, R.C., Ed., New York: Plenum, 1974, vol. 1, pp. 531–551.

    Google Scholar 

  22. Folch, J., Lees, M., and Sloane Stanley, G.H., A Simple Method for the Isolation and Purification of Total Lipids from Animal Tissues, J. Biol. Chem., 1957, vol. 226, pp. 497–509.

    PubMed  CAS  Google Scholar 

  23. Vogel H.J. A Convenient Growth Medium for Neurospora (medium N), Microbial Genet. Bull., 1956, vol. 13, pp. 42–43.

    Google Scholar 

  24. Prado-Cabrero, A., Estrada, A.F., Al-Babili, S., and Avalos, J., Identification and Biochemical Characterization of a Novel Carotenoid Oxygenase: Elucidation of the Cleavage Step in the Fusarium Carotenoid Pathway, Mol. Microbiol., 2007, vol. 64, no. 2, pp. 448–460.

    Article  PubMed  CAS  Google Scholar 

  25. Saelices, L., Youssar, L., Holdermann, I., Al-Babili, S., and Avalos, J., Identification of the Gene Responsible for Torulene Cleavage in the Neurospora Carotenoid Pathway, Mol. Genetics Genomics, 2007, vol. 278, no. 5, pp. 527–537.

    Article  CAS  Google Scholar 

  26. Prado-Cabrero, A., Schaub, P., Diaz-Sanchez, V., Estrada, A.F., Al-Babili, S., and Avalos, J., Deviation of the Neurosporaxanthin Pathway towards β-Carotene Biosynthesis in Fusarium fujikuroi by a Point Mutation in the Phytoene Desaturase Gene, FEBS J., 2009, vol. 276, pp. 4582–4597.

    Article  PubMed  CAS  Google Scholar 

  27. Strobel, I., Breitenbach, J., Scheckhuber, C.Q., Osiewacz, H.D., and Sandmann, G., Carotenoids and Carotenogenic Genes in Podospora anserina: Engineering of the Carotenoid Composition Extends the Life Span of the Mycelium, Curr. Genet., 2009, vol. 55, no. 2, pp. 175–184.

    Article  PubMed  CAS  Google Scholar 

  28. Sokolovskii, V.Yu. and Belozerskaya, T.A., Effect of Stressors on the Differential Gene Expression during Neurospora crassa Development, Usp. Biol. Khim., 2000, vol. 40, pp. 85–152.

    Google Scholar 

  29. Iigusa, H., Yoshida, Y., and Hasunuma, K., Oxygen and Hydrogen Peroxide Enhance Light-Induced Carotenoid Synthesis in Neurospora crassa, FEBS Lett., 2005, vol. 579, no. 18, pp. 4012–4016.

    Article  PubMed  CAS  Google Scholar 

  30. Langfelder, K., Streibel, M., Jahn, B., Haase, G., and Brakhage, A.A., Biosynthesis of Fungal Melanins and Their Importance for Human Pathogenic Fungi, Fungal Genet. Biol., 2003, vol. 38, pp. 143–158.

    Article  PubMed  CAS  Google Scholar 

  31. Severtsov, A.S., Napravlennost’ Evolyutsii (Directionality of Evolution), Moscow: Mos. Gos. Univ., 1990.

    Google Scholar 

  32. Rasnitsyn, A.P., Rates of Evolution and the Evolutionary Theory (Hypothesis of Adaptive Compromise), in Evolyutsiya i biotsenoticheskie krizisy (Evolution and Biocenosis Crises), Moscow: Nauka, 1987, pp. 46–64.

    Google Scholar 

  33. Nikitin, A.G. and Shmookler Reis, R.J., Role of Transposable Elements in Age-Related Genomic Instability, Genet. Res., 1997, vol. 69, no. 3, pp. 183–195.

    Article  PubMed  CAS  Google Scholar 

  34. McMurray, M.A. and Gottschling, D.E., An Age-Induced Switch to a Hyper-Recombinational State, Science, 2003, vol. 301, pp. 1908–1911.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to O. A. Kudryavtseva.

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Original Russian Text © O.A. Kudryavtseva, I.S. Mazheika, A.E. Solovchenko, O.V. Kamzolkina, 2011, published in Mikrobiologiya, 2011, Vol. 80, No. 6, pp. 772–786.

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Kudryavtseva, O.A., Mazheika, I.S., Solovchenko, A.E. et al. Genetic instability of the short-living ascomycetous fungus Podospora anserina induced by prolonged submerged cultivation. Microbiology 80, 784–796 (2011). https://doi.org/10.1134/S0026261711060105

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