DOI QR코드

DOI QR Code

Long-Term Investigation of Marine-Derived Aspergillus Diversity in the Republic of Korea

  • Jun Won Lee (School of Biological Sciences and Institute of Microbiology, Seoul National University) ;
  • Wonjun Lee (School of Biological Sciences and Institute of Microbiology, Seoul National University) ;
  • Rekhani Hansika Perera (School of Biological Sciences and Institute of Microbiology, Seoul National University) ;
  • Young Woon Lim (School of Biological Sciences and Institute of Microbiology, Seoul National University)
  • Received : 2023.08.08
  • Accepted : 2023.10.31
  • Published : 2023.12.31

Abstract

Aspergillus species play a crucial role in terrestrial environments as degraders and are well known for producing various secondary metabolites. Recently, Aspergillus species have been discovered in marine environments, exhibiting adaptability to high salinity and producing diverse secondary metabolites with valuable properties. However, limited research has focused on their marine diversity, leading to inaccurate species identification. The current study addresses this gap by investigating diverse marine habitats in the Republic of Korea, including sediment, seawater, seaweed, and marine animals. From three coasts of the Korean Peninsula, 472 Aspergillus strains were isolated from the various marine habitats. A total of 41 species were accurately identified using multigenetic markers: internal transcribed spacer, calmodulin, and b-tubulin. The findings underscore the importance of accurate identification and provide a basis for elucidating the functional role of marine-derived Aspergillus species in marine ecosystems.

Keywords

Acknowledgement

This work was supported by the management of Marine Fishery Bio-resources Center (2023), funded by the National Marine Biodiversity Institute of Korea (MABIK).

References

  1. Samson RA, Pitt JI. Integration of modern taxonomic methods for Penicillium and Aspergillus classification. FL: CRC Press; 2000.
  2. Kocsube S, Perrone G, Magista D, et al. Aspergillus is monophyletic: evidence from multiple gene phylogenies and extrolites profiles. Stud Mycol. 2016; 85(1):199-213. doi: 10.1016/j.simyco.2016.11.006.
  3. Steenwyk JL, Shen X-X, Lind AL, et al. A robust phylogenomic time tree for biotechnologically and medically important fungi in the genera Aspergillus and Penicillium. MBio. 2019;10(4):e00925-19. doi:10.1128/mBio.00925-19.
  4. Houbraken J, Kocsube S, Visagie CM, et al. Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): an overview of families, genera, subgenera, sections, series and species. Stud Mycol. 2020;95:5-169. doi: 10.1016/j.simyco.2020.05.002.
  5. de Vries RP, Visser J. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev. 2001;65(4):497-522. doi:10.1128/MMBR.65.4.497-522.2001.
  6. Hrmova M, Biely P, Vrsanska M, et al. Cellulose- and xylan-degrading enzymes of Aspergillus terreus and Aspergillus niger. Enzyme Microb Technol. 1989; 11(9):610-616. doi: 10.1016/0141-0229(89)90090-2.
  7. Planchot V, Colonna P, Gallant DJ, et al. Extensive degradation of native starch granules by alpha-amylase from Aspergillus fumigatus. J Cereal Sci. 1995; 21(2):163-171. doi: 10.1016/0733-5210(95)90032-2.
  8. Scheckermann C, Wagner F, Fischer L, et al. Galactosylation of antibiotics using the b-galactosidase from Aspergillus oryzae. Enzyme Microb Technol. 1997;20(8):629-634. doi: 10.1016/S0141-0229(96)00211-6.
  9. Yang L, Lubeck M, Lubeck PS, et al. Aspergillus as a versatile cell factory for organic acid production. Fungal Biol Rev. 2017;31(1):33-49. doi: 10.1016/j.fbr.2016.11.001.
  10. El-Hawary SS, Moawad AS, Bahr HS, et al. Natural product diversity from the endophytic fungi of the genus Aspergillus. RSC Adv. 2020; 10(37):22058-22079. doi: 10.1039/d0ra04290k.
  11. Hedayati MT, Pasqualotto AC, Warn PA, et al. Aspergillus flavus: human pathogen, allergen and mycotoxin producer. Microbiology. 2007;153(Pt 6):1677-1692. doi: 10.1099/mic.0.2007/007641-0.
  12. Damare S, Raghukumar C, Raghukumar S, et al. Fungi in deep-sea sediments of the Central Indian basin. Deep Sea Res Part I. 2006;53(1):14-27. doi:10.1016/j.dsr.2005.09.005.
  13. Kamat S, Kumari M, Taritla S, et al. Endophytic fungi of marine alga from Konkan Coast, India-a rich source of bioactive material. Front Mar Sci. 2020;7:31. doi: 10.3389/fmars.2020.00031.
  14. Lee S, Park MS, Lim YW, et al. Diversity of marinederived Aspergillus from tidal mudflats and sea sand in Korea. Mycobiology. 2016;44(4):237-247. doi: 10.5941/MYCO.2016.44.4.237.
  15. Wiese J, Ohlendorf B, Blumel M, et al. Phylogenetic identification of fungi isolated from the marine sponge Tethya aurantium and identification of their secondary metabolites. Mar Drugs. 2011;9(4):561-585. doi: 10.3390/md9040561.
  16. Jones EBG, Suetrong S, Sakayaroj J, et al. Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers. 2015;73(1):1-72. doi: 10.1007/s13225-015-0339-4.
  17. Badawy AA, Alotaibi MO, Abdelaziz AM, et al. Enhancement of seawater stress tolerance in barley by the endophytic fungus Aspergillus ochraceus. Metabolites. 2021;11(7):428. doi: 10.3390/metabo11070428.
  18. Kis-Papo T, Oren A, Wasser SP, et al. Survival of filamentous fungi in hypersaline dead sea water. Microb Ecol. 2003;45(2):183-190. doi: 10.1007/s00248-002-3006-8.
  19. Lee YM, Kim MJ, Li H, et al. Marine-derived Aspergillus species as a source of bioactive secondary metabolites. Mar Biotechnol (NY). 2013;15(5): 499-519. doi: 10.1007/s10126-013-9506-3.
  20. Orfali R, Aboseada MA, Abdel-Wahab NM, et al. Recent updates on the bioactive compounds of the marine-derived genus Aspergillus. RSC Adv. 2021;11(28):17116-17150. doi: 10.1039/d1ra01359a.
  21. Jones EG, Pang KL. Marine fungi: and fungal-like organisms. Berlin (Germany): Walter de Gruyter; 2012.
  22. Samson RA, Visagie CM, Houbraken J, et al. Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol. 2014;78(1):141-173. doi: 10.1016/j.simyco.2014.07.004.
  23. Lee S, Park MS, Lee H, et al. Fungal diversity and enzyme activity associated with the macroalgae, Agarum clathratum. Mycobiology. 2019;47(1):50-58. doi: 10.1080/12298093.2019.1580464.
  24. Lee W, Kim JS, Seo CW, et al. Diversity of Cladosporium (Cladosporiales, Cladosporiaceae) species in marine environments and report on five new species. MycoKeys. 2023a;98:87-111. doi: 10.3897/mycokeys.98.101918.
  25. R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2022. Available from: http://www.R-project.org/.
  26. Kahle DJ, Wickham H. GGMAP: spatial visualization with ggplot2. The R J. 2013;5(1):144-161. doi:10.32614/RJ-2013-014.
  27. White TJ. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocol Guide Method Appl. 1990;18(1):315-322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  28. Glass NL, Donaldson GC. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol. 1995;61(4):1323-1330. doi: 10.1128/aem.61.4.1323-1330.1995.
  29. Hong S-B, Go S-J, Shin H-D, et al. Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia. 2005;97(6):1316-1329. doi: 10.1080/15572536.2006.11832738.
  30. Peterson SW. Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia. 2008;100(2):205-226. doi: 10.1080/15572536.2008.11832477.
  31. Kearse M, Moir R, Wilson A, et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647-1649. doi: 10.1093/bioinformatics/bts199.
  32. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-780. doi: 10.1093/molbev/mst010.
  33. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312-1313. doi:10.1093/bioinformatics/btu033.
  34. Varga J, Frisvad JC, Kocsube S, et al. New and revisited species in Aspergillus section Nigri. Stud Mycol. 2011;69(1):1-17. doi: 10.3114/sim.2011.69.01.
  35. Bian C, Kusuya Y, Sklenar F, et al. Reducing the number of accepted species in Aspergillus series Nigri. Stud Mycol. 2022;102(1):95-132. doi: 10. 3114/sim.2022.102.03. https://doi.org/10.3114/sim.2022.102.03
  36. Sklenar F, Jurjevic Z, Houbraken J, et al. Re-examination of species limits in Aspergillus section Flavipedes using advanced species delimitation methods and description of four new species. Stud Mycol. 2021;99(1):100120-100120. doi: 10.1016/j. simyco.2021.100120.
  37. Sklenar F, Glassnerova K, Jurjevic Z, et al. Taxonomy of Aspergillus series Versicolores: species reduction and lessons learned about intraspecific variability. Stud Mycol. 2022;102(1):53-93. doi: 10.3114/sim.2022.102.02.
  38. Araujo CA, Ferreira PC, Pupin B, et al. Osmotolerance as a determinant of microbial ecology: a study of phylogenetically diverse fungi. Fungal Biology. 2020;124(5):273-288. doi: 10.1016/j.funbio.2019.09.001.
  39. Cai L, Xu S, Lu T, et al. Salt-tolerant mechanism of marine Aspergillus niger cellulase cocktail and improvement of its activity. Chin J Chem Eng. 2020;28(4):1120-1128. doi: 10.1016/j.cjche.2019.11.012.
  40. Jalili B, Bagheri H, Azadi S, et al. Identification and salt tolerance evaluation of endophyte fungi isolates from halophyte plants. Int J Environ Sci Technol. 2020;17(7):3459-3466. doi: 10.1007/s13762-020-02626-y.
  41. Abdel-Azeem AM, Abdel-Azeem MA, Abdul-Hadi SY et al. Aspergillus: biodiversity, ecological significances, and industrial applications. In Mishra S, Singh S, Gupta A, et al., editors, Recent advancement in white biotechnology through fungi: volume 1: diversity and enzymes perspectives. Cham; Germany: Springer; 2019. p. 121-179.
  42. Espinosa SKC, et al. Phylogenetic identification, diversity, and richness of Aspergillus from homes in Havana, Cuba. Microorganisms. 2021;9(1):115.
  43. Jamy M, Biwer C, Vaulot D, et al. Global patterns and rates of habitat transitions across the eukaryotic tree of life. Nat Ecol Evol. 2022;6(10):1458-1470. doi: 10.1038/s41559-022-01838-4.
  44. Chang KI, Zhang CI, Park C, et al. Oceanography of the east sea (Japan Sea). Cham: Springer International Publishing; 2016. p. 17.
  45. Koh CH, Khim JS. The Korean tidal flat of the yellow sea: physical setting, ecosystem and management. Ocean Coastal Manage. 2014;102:398-414. doi: 10.1016/j.ocecoaman.2014.07.008.
  46. Baek SH. First report for appearance and distribution patterns of the epiphytic dinoflagellates in the Korean Peninsula. Korean J Environ Biol. 2012; 30(4):355-361. doi: 10.11626/KJEB.2012.30.4.355.
  47. Seo MH, Choi SY, Park E-O, et al. Species diversity of planktonic copepods and distribution characteristics of its major species in coastal waters of Korea. Korean J Environ Biol. 2018;36(4):525-537. doi: 10.11626/KJEB.2018.36.4.525.
  48. Lee JW, Seo CW, Lee W, et al. Diversity and dynamics of marine arenicolous fungi in three seasides of the Korean peninsula. J Microbiol. 2023b; 61(1):63-82. doi: 10.1007/s12275-023-00011-1.
  49. Jones EG. Marine fungi: some factors influencing biodiversity. Fungal Divers. 2000;4:53-73.
  50. Li P-D, Jeewon R, Aruna B, et al. Metabarcoding reveals differences in fungal communities between unflooded versus tidal flat soil in coastal saline ecosystem. Sci Total Environ. 2019;690:911-922. doi: 10.1016/j.scitotenv.2019.06.473.
  51. Lv X, Ma B, Yu J, et al. Bacterial community structure and function shift along a successional series of tidal flats in the yellow river delta. Sci Rep. 2016;6(1):36550. doi: 10.1038/srep36550.
  52. Moustafa AF, Sharkas MS. Fungi associated with cellulose decomposition in the tidal mud-flats of Kuwait. Mycopathologia. 1982;78(3):185-190. doi: 10.1007/BF00466074.
  53. Harvell D, Jordan-Dahlgren E, Merkel S, et al. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanog. 2007;20(1):172-195. doi: 10.5670/oceanog.2007.91.
  54. Zuluaga-Montero A, Toledo-Hernandez C, Rodriguez JA, et al. Spatial variation in fungal communities isolated from healthy and diseased sea fans Gorgonia ventalina and seawater. Aquat Biol. 2010;8(2):151-160. doi: 10.3354/ab00218.
  55. Bonugli-Santos RC, Dos Santos Vasconcelos MR, Passarini MRZ, et al. Marine-derived fungi: diversity of enzymes and biotechnological applications. Front Microbiol. 2015;6:269. doi: 10.3389/fmicb.2015.00269.
  56. Harpke M, Pietschmann S, Ueberschaar N, et al. Salt and metal tolerance involves formation of guttation droplets in species of the Aspergillus versicolor complex. Genes. 2022;13(9):1631. doi: 10. 3390/genes13091631. https://doi.org/10.3390/genes13091631
  57. Rodriguez-Pupo EC, Perez-Llano Y, TinocoValencia JR, et al. Osmolyte signatures for the protection of Aspergillus sydowii cells under halophilic conditions and osmotic shock. JoF. 2021;7(6):414. doi: 10.3390/jof7060414.
  58. Patyshakuliyeva A, Falkoski DL, Wiebenga A, et al. Macroalgae derived fungi have high abilities to degrade algal polymers. Microorganisms. 2019;8(1):52. doi: 10.3390/microorganisms8010052.
  59. Suryanarayanan TS. Fungal endosymbionts of seaweeds. In: Raghukumar C, editor, Biology of marine fungi. Berlin (Germany): Springer; 2011. p. 53-69.
  60. Suryanarayanan TS, Venkatachalam A, Thirunavukkarasu N, et al. Internal mycobiota of marine macroalgae from the Tamilnadu coast: distribution, diversity and biotechnological potential. De Gruyter. 2010;53(5):457-468. https://doi.org/10.1515/bot.2010.045
  61. Zuccaro A, Schoch CL, Spatafora JW, et al. Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Appl Environ Microbiol. 2008;74(4):931-941. https://doi.org/10.1128/AEM.01158-07
  62. Park MS, Oh S-Y, Lee S, et al. Fungal diversity and enzyme activity associated with sailfin sandfish egg masses in Korea. Fungal Ecol. 2018;34:1-9. doi: 10.1016/j.funeco.2018.03.004.