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Diversity and enzyme activity of Penicillium species associated with macroalgae in Jeju Island

  • Microbial Systematics and Evolutionary Microbiology
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Abstract

A total of 28 strains of 19 Penicillium species were isolated in a survey of extracellular enzyme-producing fungi from macroalgae along the coast of Jeju Island of Korea. Penicillium species were identified based on morphological and β-tubulin sequence analyses. In addition, the halo-tolerance and enzyme activity of all strains were evaluated. The diversity of Penicillium strains isolated from brown algae was higher than the diversity of strains isolated from green and red algae. The commonly isolated species were Penicillium antarcticum, P. bialowiezense, P. brevicompactum, P. crustosum, P. oxalicum, P. rubens, P. sumatrense, and P. terrigenum. While many strains showed endoglucanase, β-glucosidase, and protease activity, no alginase activity was detected. There was a positive correlation between halo-tolerance and endoglucanase activity within Penicillium species. Among 19 Penicillium species, three species–P. kongii, P. olsonii, and P. viticola–have not been previously recorded in Korea.

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References

  • Adsul, M.G., Ghule, J.E., Singh, R., Shaikh, H., Bastawde, K.B., Gokhale, D.V., and Varma, A.J. 2004. Polysaccharides from bagasse: applications in cellulase and xylanase production. Carbohydr. Polym. 57, 67–72.

    Article  CAS  Google Scholar 

  • Agarwal, D., Patidar, P., Banerjee, T., and Shridhar, P. 2004. Production of alkaline protease by Penicillium sp. under SSF conditions and its application to soy protein hydrolysis. Process Biochem. 39, 1–6.

    Google Scholar 

  • Benjamini, Y. and Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B. 57, 289–300.

    Google Scholar 

  • Bugni, T.S. and Ireland, C.M. 2004. Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat. Prod. Rep. 21, 143–163.

    Article  CAS  PubMed  Google Scholar 

  • Burtseva, Y.V., Sova, V., Pivkin, M., Anastyuk, S., Gorbach, V., and Zvyagintseva, T. 2010. Distribution of O-glycosylhydrolases in marine fungi of the Sea of Japan and the Sea of Okhotsk: characterization of exocellular N-acetyl-ß-D-glucosaminidase of the marine fungus Penicillium canescens. Appl. Biochem. Microbiol. 46, 648–656.

    Article  CAS  Google Scholar 

  • Cantrell, S.A., Casillas-Martínez, L., and Molina, M. 2006. Characterization of fungi from hypersaline environments of solar salterns using morphological and molecular techniques. Mycol. Res. 110, 962–970.

    Article  CAS  PubMed  Google Scholar 

  • Chanda, S., Dave, R., Kaneria, M., and Nagani, K. 2010. Seaweeds: a novel, untapped source of drugs from sea to combat infectious diseases. In Mendez-Vilas, A. (ed.), Current research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. Formatex Research Center, Badajoz, Spain.

    Google Scholar 

  • Damare, S., Raghukumar, C., Muraleedharan, U.D., and Raghukumar, S. 2006. Deep-sea fungi as a source of alkaline and coldtolerant proteases. Enzyme Microb. Technol. 39, 172–181.

    Article  CAS  Google Scholar 

  • Domozych, D.S. 2011. Algal cell walls. In eLS. John Wiley & Sons Ltd., Chichester, UK.

    Book  Google Scholar 

  • Dubrovskaya, Y.V., Sova, V., Slinkina, N., Anastyuk, S., Pivkin, M., and Zvyagintseva, T. 2012. Extracellular ß-D-glucosidase of the Penicillium canescens marine fungus. Appl. Biochem. Microbiol. 48, 401–408.

    Article  CAS  Google Scholar 

  • Dunn, P.H. and Baker, G.E. 1983. Filamentous fungi of the psammon habitat at Enewetak Atoll, Marshall Islands. Mycologia 75, 839–853.

    Article  Google Scholar 

  • Dutta, T., Sahoo, R., Sengupta, R., Ray, S.S., Bhattacharjee, A., and Ghosh, S. 2008. Novel cellulases form an extremophilic filamentous fungi Penicillium citrinum: production and characterization. J. Ind. Microbiol. Biotechnol. 35, 275–282.

    Article  CAS  PubMed  Google Scholar 

  • Frisvad, J.C. and Samson, R.A. 2004. Polyphasic taxonomy of Penicillium subgenus Penicillium. A guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Stud. Mycol. 49, 1–174.

    Google Scholar 

  • Germano, S., Pandey, A., Osaku, C.A., Rocha, S.N., and Soccol, C.R. 2003. Characterization and stability of protease from Penicillium sp. produced by solid-state fermentation. Enzyme Microb. Technol. 32, 246–251.

    Article  CAS  Google Scholar 

  • Glass, N.L. and Donaldson, G.C. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61, 1323–1330.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Graham, L.E., Graham, J.M., and Wilcox, L.W. 2009. Algae. 2nd ed. Pearson/Benjamin Cummings, San Francisco, California, USA.

    Google Scholar 

  • Houbraken, J. and Samson, R. 2011. Phylogeny of Penicillium and the segregation of Trichocomaceae into three families. Stud. Mycol. 70, 1–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, X.L., Gao, Y., Xue, D.Q., Liu, H.L., Peng, C.S., Zhang, F.L., Li, Z.Y., and Guo, Y.W. 2011. Streptomycindole, an indole alkaloid from a marine Streptomyces sp. DA22 associated with South China Sea Sponge Craniella australiensis. Helvetica Chimica Acta. 94, 1838–1842.

    CAS  Google Scholar 

  • Hyde, K.D., Jones, E.B.G., Leano, E., Pointing, S.B., Poonyth, A.D., and Vrijmoed, L.L.P. 1998. Role of fungi in marine ecosystems. Biodivers. Conserv. 7, 1147–1161.

    Article  Google Scholar 

  • Iwamoto, C., Minoura, K., Hagishita, S., Oka, T., Ohta, T., Hagishita, S., and Numata, A. 1999. Absolute sterostructures of novel penostatins A–E from a Penicillium species from an Enteromorpha marine alga. Tetrahedron 55, 14353–14368.

    Article  CAS  Google Scholar 

  • Janso, J.E., Bernan, V.S., Greenstein, M., Bugni, T.S., and Ireland, C.M. 2005. Penicillium dravuni, a new marine-derived species from an alga in Fiji. Mycologia 97, 444–453.

    Article  CAS  PubMed  Google Scholar 

  • Jo, G.H., Jung, W.J., Kuk, J.H., Oh, K.T., Kim, Y.J., and Park, R.D. 2008. Screening of protease-producing Serratia marcescens FS-3 and its application to deproteinization of crab shell waste for chitin extraction. Carbohydr. Polym. 74, 504–508.

    Article  CAS  Google Scholar 

  • Kang, J.C., Choi, H.G., and Kim, M.S. 2011. Macroalgal species composition and seasonal variation in biomass on Udo, Jeju Island, Korea. Algae 26, 333–342.

    Article  Google Scholar 

  • Kang, E.J., Kim, J.H., Kim, K., Choi, H.G., and Kim, K.Y. 2014. Reevaluation of green tide-forming species in the Yellow Sea. Algae 29, 267–277.

    Article  Google Scholar 

  • Khudyakova, Y.V., Pivkin, M.V., Kuznetsova, T.A., and Svetashev, V.I. 2000. Fungi in sediments of the sea of Japan and their biologically active metabolites. Microbiology 69, 608–611.

    Article  CAS  Google Scholar 

  • Kim, W.G., Koo, H.M., Kim, K.H., Hyun, I.H., Hong, S.K., Cha, J.S., and Kim, D.G. 2009. List of plant diseases in Korea. Korean Society of Plant Pathology, Suwon, Korea.

    Google Scholar 

  • Kohlmeyer, J. and Kohlmeyer, E. 1979. Marine Mycology. Academic Press, New York, USA.

    Google Scholar 

  • Kornerup, A. and Wanscher, J.H. 1963. Methuen handbook of colour. Methuen. London, UK.

    Google Scholar 

  • Krogh, K.B.R., Mørkeberg, A., Jørgensen, H., Frisvad, J.H.C., and Olsson, L. 2004. Screening genus Penicillium for producers of cellulolytic and xylanolytic enzymes. Appl. Biochem. Biotechnol. 114, 389–401.

    Article  Google Scholar 

  • Lee, Y. 2008. Marine algae of Jeju. Academy Press, Seoul.

    Google Scholar 

  • Lee, S., Hong, S.B., and Kim, C.Y. 2003. Contribution to the checklist of soil-inhabiting fungi in Korea. Mycobiology 31, 9–18.

    Article  Google Scholar 

  • Lee, H., Lee, Y.M., Heo, Y.M., Lee, H., Hong, J.H., Jang, S., Park, M.S., Lim, Y.W., and Kim, J.J. 2015. Halo-tolerance of marine-derived fungi and their enzymatic properties. Bioresources 10, 8450–8460.

    CAS  Google Scholar 

  • Li, Q. and Wang, G. 2009. Diversity of fungal isolates from three Hawaiian marine sponges. Microbiol. Res. 164, 233–241.

    Article  CAS  PubMed  Google Scholar 

  • Numata, A., Takahashi, C., Ito, Y., Minoura, K., Yamada, T., Matsuda, C., and Nomoto, K. 1996. Penochalasins, a novel class of cytotoxic cytochalasans from a Penicillium species separated from a marine alga: structure determination and solution conformation. J. Chem. Soc. Perkin. Trans. 1, 239–245.

    Article  Google Scholar 

  • Park, M.S., Eom, J.E., Fong, J.J., and Lim, Y.W. 2015. New record and enzyme activity of four species in Penicillium section Citrina from marine environments in Korea. J. Microbiol. 53, 219–225.

    Article  CAS  PubMed  Google Scholar 

  • Park, M.S., Fong, J.J., Oh, S.Y., Kwon, K.K., Sohn, J.H., and Lim, Y.W. 2014. Marine-derived Penicillium in Korea: diversity, enzyme activity, and antifungal properties. Antonie van Leeuwenhoek 106, 331–345.

    Article  CAS  PubMed  Google Scholar 

  • Paz, Z., Komon-Zelazowska, M., Druzhinina, I., Aveskamp, M., Shnaiderman, A., Aluma, Y., Carmeli, S., Ilan, M., and Yarden, O. 2010. Diversity and potential antifungal properties of fungi associated with a Mediterranean sponge. Fungal Divers. 42, 17–26.

    Article  Google Scholar 

  • Pisano, M.A., Mihalik, J.A., and Catalano, G.R. 1964. Gelatinase activity by marine fungi. Appl. Environ. Microbiol. 12, 470–474.

    CAS  Google Scholar 

  • Pitt, J.I. 1979. The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic Press, London, UK.

    Google Scholar 

  • Pointing, S.B. 1999. Qualitative methods for the determination of lignocellulolytic enzyme production by tropical fungi. Fungal Divers. 2, 17–33.

    Google Scholar 

  • Popper, Z.A., Michel, G., Hervé, C., omozych, D.S., Willats, W.G.T., Tuohy, M.G., Kloareg, B., and Stengel, D.B. 2011. Evolution and diversity of plant cell walls: from algae to flowering plants. Annu. Rev. Plant Biol. 62, 567–590.

    Article  CAS  PubMed  Google Scholar 

  • Raghukumar, C. 2008. Marine fungal biotechnology: an ecological perspective. Fungal Divers. 31, 19–35.

    Google Scholar 

  • Ristanovic, B. and Miller, C.E. 1969. Salinity tolerances and ecological aspects of some fungi collected from fresh-water, estuarine and marine habitats. Mycopath. Mycol. Appl. 37, 273–280.

    Article  Google Scholar 

  • Rogers, S.O. and Bendich, A.J. 1994. Extraction of total cellular DNA from plants, algae and fungi. In Gelvin, S. and Schilperoort, R. (eds.), Plant molecular biology manual, Kluwer Academic, Dordrecht, Netherlands.

  • Samson, R.A., Houbraken, J., Thrane, U., Frisvad, J.C., and Andersen, B. 2010. Food and indoor fungi. CBS-Fungal Biodiversity Centre Utrecht, Netherlands.

    Google Scholar 

  • Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.

    Article  CAS  PubMed  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teng, W.L., Khor, E., Tan, T.K., and Tan, S.C. 2001. Concurrent production of chitin from shrimp shells and fungi. Carbohydr. Res. 332, 305–316.

    Article  CAS  PubMed  Google Scholar 

  • Vansteelandt, M., Kerzaon, I., Blanchet, E., Tankoua, O.F., Du Pont, T.R., Joubert, Y., and Grovel, O. 2012. Patulin and secondary metabolite production by marine-derived Penicillium strains. Fungal Biol. 116, 954–961.

    Article  CAS  PubMed  Google Scholar 

  • Visagie, C.M., Houbraken, J., Frisvad, J.C., Hong, S.B., Klaassen, C.H.W., Perrone, G., Seifert, K.A., Varga, J., Yaguchi, T., and Samson, R.A. 2014. Identification and nomenclature of the genus Penicillium. Stud. Mycol. 78, 343–371.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, S.L. and Chio, S.H. 1998. Deproteinization of shrimp and crab shell with the protease of Pseudomonas aeruginosa K-187. Enzyme Microb. Technol. 22, 629–633.

    Article  CAS  Google Scholar 

  • Yoon, J.H., Hong, S.B., Ko, S.J., and Kim, S.H. 2007. Detection of extracellular enzyme activity in Penicillium using chromogenic media. Mycobiology 35, 166–169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, S.H. 2006. Penicillium species associated with post-harvest diseases of plant products. National Institute of Agricultural Science and Technology, Suwon, Korea.

    Google Scholar 

  • Zuccaro, A., Summerbell, R.C., Gams, W., Schroers, H.J., and Mitchell, J.I. 2004. A new Acremonium species associated with Fucus spp., and its affinity with a phylogenetically distinct marine Emericellopsis clade. Stud. Mycol. 50, 283–297.

    Google Scholar 

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Authors and Affiliations

  1. School of Biological Sciences, Seoul National University, Seoul, 08826, Republic of Korea

    Myung Soo Park, Seobihn Lee, Seung-Yoon Oh & Young Woon Lim

  2. National Institute of Biological Resources, Environmental Research Complex, Incheon, 22689, Republic of Korea

    Ga Youn Cho

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  1. Myung Soo Park
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  2. Seobihn Lee
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Park, M.S., Lee, S., Oh, SY. et al. Diversity and enzyme activity of Penicillium species associated with macroalgae in Jeju Island. J Microbiol. 54, 646–654 (2016). https://doi.org/10.1007/s12275-016-6324-0

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