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Isolation and characterization of bioactive fungi from shark Carcharodon carcharias’ gill with biopharmaceutical prospects

  • Chemistry
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Until recently, little was known about the fungi found in shark gills and their biomedicinal potential. In this article, we described the isolation, bioactivity, diversity, and secondary metabolites of bioactive fungi from the gill of a shark (Carcharodon carcharias). A total of 115 isolates were obtained and grown in 12 culture media. Fifty-eight of these isolates demonstrated significant activity in four antimicrobial, pesticidal, and cytotoxic bioassay models. Four randomly selected bioactive isolates inhibited human cancer cell proliferation during re-screening. These active isolates were segregated into 6 genera using the internal transcribed spacer-large subunit (ITS-LSU) rDNA-sequence BLAST comparison. Four genera, Penicillium, Aspergillus, Mucor, and Chaetomium were the dominant taxa. A phylogenic tree illustrated their intergenera and intragenera genetic diversity. HPLC-DAD-HRMS analysis and subsequent database searching revealed that nine representative strains produced diverse bioactive compound profiles. These results detail the broad range of bioactive fungi found in a shark’s gills, revealing their biopharmaceutical potential. To the best of our knowledge, this is the first study characterizing shark gill fungi and their bioactivity.

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References

  • Abbott W S. 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol., 18 (2): 265–267.

    Article  Google Scholar 

  • Alam M Z, Ahmad S, Malik A. 2009. Genotoxic and mutagenic potential of agricultural soil irrigated with tannery effluents at Jajmau (Kanpur), India. Arch. Environ. Contam. Toxicol., 57 (3): 463–476.

    Article  Google Scholar 

  • Armstrong E, Yan L M, Boyd K G, Wright P C, Burgess J G. 2001. The symbiotic role of marine microbes on living surfaces. Hydrobiologia, 461 (1-3): 37–40.

    Article  Google Scholar 

  • Baker P W, Kennedy J, Dobson A D, Marchesi J R. 2009. Phylogenetic diversity and antimicrobial activities of fungi associated with Haliclona simulans isolated from Irish coastal waters. Mar. Biotechnol., 11 (4): 540–547.

    Article  Google Scholar 

  • Bartus H R, Mirabelli C K, Auerbach J I, Shatzman A R, Taylor D P, Johnson R K, Rosenberg M, Crooke S T. 1984. Improved genetically modified Escherichia coli strain for prescreening antineoplastic agents. Antimicrob. Agents. Chemother., 25 (5): 622–625.

    Article  Google Scholar 

  • Blunt J W, Copp B R, Munro M H, Northcote P T, Prinsep M R. 2011. Marine natural products. Nat. Prod. Rep., 28 (2): 196–268.

    Article  Google Scholar 

  • Buckingham J. 2011. Dictionary of Natural Products on DVD. version 20: 2. Chapman and Hall/CRC, London.

    Google Scholar 

  • Bugni T S, Ireland C M. 2004. Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat. Prod. Rep., 21 (1): 143–163.

    Article  Google Scholar 

  • Carballo J L, Herná ndez-Inda Z L, Pérez P, García-Grávalos M D. 2002. A comparison between two brine shrimp assays to detect in vitro cytotoxicity in marine natural products. BMC Biotechnol., 2: 17.

    Article  Google Scholar 

  • De Maddalena A. 2007. Great White Sharks Preserved in European Museums. Cambridge Scholars Publishing, Newcastle.

    Google Scholar 

  • Ding B, Yin Y, Zhang F L, Li Z Y. 2011. Recovery and phylogenetic diversity of culturable fungi associated with marine sponges Clathrina luteoculcitella and Holoxea sp. in the South China Sea. Mar. Biotechnol., 13 (4): 713–721.

    Article  Google Scholar 

  • Du L, Feng T, Zhao B Y, Li D H, Cai S X, Zhu T J, Wang F P, Xiao X, Gu Q Q. 2010. Alkaloids from a deep ocean sediment-derived fungus Penicillium sp. and their antitumor activities. J. Antibiot. ( Tokyo ), 63 (4): 165–170.

    Article  Google Scholar 

  • Hentschel U, Piel J, Degnan S M, Taylor M W. 2012. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol., 10 (9): 641–654.

    Article  Google Scholar 

  • Hu Z Y, Liu S Z, Huang H, Huang C S, Su W J. 2000. A rapid screening assay for insecticidal antibiotic produced by marine actinomycetes. Mar. Sci. Bul. ( Haiyang Tongbao ), 19 (4): 36–41. (in Chinese with English abstract)

    Google Scholar 

  • Knickle C, Billingsley L, DiVittorio K. 2011. Biological profiles basking shark. Florida Museum of Natural History. http://www.flmnh.ufl.edu/fish/Gallery/Descript/ baskingshark/baskingshark.html. Retrieved 2011-12-21.

    Google Scholar 

  • Kobayashi H, Namikoshi M, Yoshimoto T, Yokochi T. 1996. A screening method for antimitotic and antifungal substances using conidia of Pyricularia oryzae, modification and application to tropical marine fungi. J. Antibiot. ( Tokyo ), 49 (9): 873–879.

    Article  Google Scholar 

  • Kobayashi J, Ishibashi M. 1993. Bioactive metabolites of symbiotic marine microorganisms. Chem. Rev., 93 (5): 1 753–1 769.

  • Li G, Lin Y. 2004. Differential DNA repair test for screening of the anti-tumor marine microorganisms. Chin. J. Antibiot. ( Zhongguo Kangshengsu Zazhi ), 29 (8): 449–451. (in Chinese with English abstract)

    Google Scholar 

  • Menezes C B A, Bonugli-Santos R C, Miqueletto P B, Passarini M R Z, Silva C H, Justo M R, Leal R R, Fantinatti-Garboggini F, Oliveira V M, Berlinck R G S, Sette L D. 2010. Microbial diversity associated with algae, ascidians and sponges from the north coast of São Paulo state, Brazil. Microbiol. Res., 165 (6): 466–482.

    Article  Google Scholar 

  • Meng Q W, Su J X, Li W D. 1987. Comparative Anatomy of Fish. Science Press, Beijing. (in Chinese)

    Google Scholar 

  • Mohammed Y S, Luckner M. 1963. The structure of cyclopenin and cyclopenol, metabolic products from P enicillium cyclopium westling and P enicillium viridicatum westling. Tetrahedron Lett., 4 (28): 1 953–1 958.

    Article  Google Scholar 

  • Mueller H, Kassack M U, Wiese M. 2004. Comparison of the usefulness of the MTT, ATP, and calcein assays to predict the potency of cytotoxic agents in various human cancer cell lines. J. Biomol. Screen., 9 (6): 506–515.

    Article  Google Scholar 

  • Passarini M R Z, Santos C, Lima N, Berlinck R G S, Sette L D. 2013. Filamentous fungi from the Atlantic marine sponge Dragmacidon reticulatum. Arch. Microbiol., 195 (2): 99–111.

    Article  Google Scholar 

  • Peterson S W. 2012. Aspergillus and Penicillium identification using DNA sequences: barcode or MLST? Appl. Microbiol. Biotechnol., 95 (2): 339–344.

    Article  Google Scholar 

  • Pieter S S, Robert V. 1983. Roquefortine, an intermediate in the biosynthesis of oxaline in cultures of Penicillium oxalicum. J. Chem. Soc., Chem. Comm., (10): 560–561.

    Google Scholar 

  • Pinkerton F, Strobel G. 1976. Serinol as an activator of toxin production in attenuated cultures of Helminthosporium sacchari. Proc. Natl. Acad. Sci. U. S. A., 73 (11): 4 007–4 011.

    Article  Google Scholar 

  • Proksch P, Putz A, Ortlepp S, Kjer J, Bayer M. 2010. Bioactive natural products from marine sponges and fungal endophytes. Phytochem. Rev., 9 (4): 475–489.

    Article  Google Scholar 

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

    Google Scholar 

  • Strobel G, Yang X, Sears J, Kramer R, Sidhu R S, Hess W M. 1996. Taxol from Pestalotiopsis microspora, an endophytic fungus of Taxus wallachiana. Microbiology, 142 (2): 435–440.

    Article  Google Scholar 

  • Swathi J, Narendra K, Sowjanya K M, Satya A K. 2013. Marine fungal metabolites as a rich source of bioactive compounds. Afr. J. Biochem. Res., 7 (10): 184–196.

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol., 24 (8): 1 596–1 599.

    Article  Google Scholar 

  • Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic. Acids. Res., 25 (24): 4 876–4 882.

    Article  Google Scholar 

  • White T J, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M A G D, Sninsky J J, White T J eds. Pcr Protocols: A Guide to Methods and Applications. 1 st edn. Academic Press, New York. p.315–322.

    Google Scholar 

  • Wiese J, Ohlendorf B, Blümel M, Schmaljohann R, Imhoff J F. 2011. Phylogenetic identification of fungi isolated from the marine sponge Tethya aurantium and identification of their secondary metabolites. Mar. Drugs, 9 (4): 561–585.

    Article  Google Scholar 

  • Xin Z H, Fang Y, Du L, Zhu T, Duan L, Chen J, Gu Q Q, Zhu W M. 2007. Aurantiomides A-C, quinazoline alkaloids from the sponge-derived fungus Penicillium aurantiogriseum SP0-19. J. Nat. Prod., 70 (5): 853–855.

    Article  Google Scholar 

  • Xiong L, Li J, Kong F. 2004. Streptomyces sp. 173, an insecticidal micro-organism from marine. Lett. Appl. Microbiol., 38 (1): 32–37.

    Google Scholar 

  • Xu Y J, Yan X J. 2006. Research advances in chemical ecology of marine microorganisms. Chin. J. Appl. Ecol., 17 (12): 2 436–2 440. (in Chinese with English abstract)

    Google Scholar 

  • Zhang Y, Mu J, Han J, Gu X. 2012. An improved brine shrimp larvae lethality microwell test method. Toxicol. Mech. Methods., 22 (1): 23–30.

    Article  Google Scholar 

  • Zhou K, Zhang X, Zhang F L, Li Z Y. 2011. Phylogenetically diverse cultivable fungal community and polyketide synthase (PKS), non-ribosomal peptide synthase (NRPS) genes associated with the South China Sea sponges. Microb. Ecol., 62 (3): 644–654.

    Article  Google Scholar 

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Authors and Affiliations

  1. College of Food Science and Technology, Guangdong Ocean University, Guangdong Provincial Key Laboratory of Aquatic Product Processing and Safety, Key Laboratory of Advanced Processing of Aquatic Products of Guangdong Higher Education Institution, Zhanjiang, 524088, China

    Yi Zhang  (张翼) & Yan Feng  (冯妍)

  2. School of Environmental and Chemical Engineering, Dalian Jiaotong University, Dalian, 116028, China

    Yi Zhang  (张翼), Jinyuan Han  (韩金媛) & Haiyan Bao  (鲍海燕)

  3. School of Life Science and Biotechnology, Dalian University of Technology, Dalian, 116024, China

    Yi Zhang  (张翼)

  4. Institute of Organic Chemistry, University of Tübingen, Tübingen, 72076, Germany

    Yi Zhang  (张翼) & Stephanie Grond

  5. Marine Science and Technology College, Zhejiang Ocean University, Zhoushan, 316022, China

    Jun Mu  (穆军)

  6. Inter - Faculty Institute for Microbiology and Infectious Medicine, University of Tübingen, Tübingen, 72076, Germany

    Andreas Kulik

Authors
  1. Yi Zhang  (张翼)
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  2. Jinyuan Han  (韩金媛)
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  3. Yan Feng  (冯妍)
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  4. Jun Mu  (穆军)
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  5. Haiyan Bao  (鲍海燕)
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  6. Andreas Kulik
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  7. Stephanie Grond
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Corresponding authors

Correspondence to Yi Zhang  (张翼), Jun Mu  (穆军) or Stephanie Grond.

Additional information

Supported by the National Natural Science Foundation of China (No. 20902009), the National Science Foundation for Post-Doctoral Scientists of China (Nos. 2011M500051, 2012T50258), the YangFan Scarce Top Talent Project of Guangdong Province (to ZHANG Yi), the Program for Scientific Research Start-up Funds of Guangdong Ocean University (GDOU) (to ZHANG Yi), and the Natural Science Research Project of GDOU (No. C14519)

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Zhang, Y., Han, J., Feng, Y. et al. Isolation and characterization of bioactive fungi from shark Carcharodon carcharias’ gill with biopharmaceutical prospects. Chin. J. Ocean. Limnol. 34, 186–199 (2016). https://doi.org/10.1007/s00343-015-4187-6

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  • DOI: https://doi.org/10.1007/s00343-015-4187-6

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