Mycobiology

  • 제49권2호
  • /
  • Pages.151-160
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  • 2021
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  • 1229-8093(pISSN)
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  • 2092-9323(eISSN)
한국균학회 (The Korean Society of Mycology)
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Diversity and Antiaflatoxigenic Activities of Culturable Filamentous Fungi from Deep-Sea Sediments of the South Atlantic Ocean

  • Zhou, Ying (School of Marine Science and Technology, Harbin Institute of Technology) ;
  • Gao, Xiujun (School of Marine Science and Technology, Harbin Institute of Technology) ;
  • Shi, Cuijuan (School of Marine Science and Technology, Harbin Institute of Technology) ;
  • Li, Mengying (School of Marine Science and Technology, Harbin Institute of Technology) ;
  • Jia, Wenwen (School of Marine Science and Technology, Harbin Institute of Technology) ;
  • Shao, Zongze (China Key Laboratory of Marine Genetic Resources, The Third Institute of Oceanography, Ministry of Natural Resources) ;
  • Yan, Peisheng (School of Marine Science and Technology, Harbin Institute of Technology)
  • 투고 : 2020.07.14
  • 심사 : 2020.12.28
  • 발행 : 2021.04.30
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초록

Despite recent studies, relatively few are known about the diversity of fungal communities in the deep Atlantic Ocean. In this study, we investigated the diversity of fungal communities in 15 different deep-sea sediments from the South Atlantic Ocean with a culture-dependent approach followed by phylogenetic analysis of ITS sequences. A total of 29 fungal strains were isolated from the 15 deep-sea sediments. These strains belong to four fungal genera, including Aspergillus, Cladosporium, Penicillium, and Alternaria. Penicillium, accounting for 44.8% of the total fungal isolates, was a dominant genus. The antiaflatoxigenic activity of these deep-sea fungal isolates was studied. Surprisingly, most of the strains showed moderate to strong antiaflatoxigenic activity. Four isolates, belonging to species of Penicillium polonicum, Penicillium chrysogenum, Aspergillus versicolor, and Cladosporium cladosporioides, could completely inhibit not only the mycelial growth of Aspergillus parasiticus mutant strain NFRI-95, but also the aflatoxin production. To our knowledge, this is the first report to investigate the antiaflatoxigenic activity of culturable deep-sea fungi. Our results provide new insights into the community composition of fungi in the deep South Atlantic Ocean. The high proportion of strains that displayed antiaflatoxigenic activity demonstrates that deep-sea fungi from the Atlantic Ocean are valuable resources for mining bioactive compounds.

키워드

과제정보

This work was supported by National Natural Science Foundation of China [Grant No. 31900088], COMRA program [DY135-B2-17], the Fundamental Research Funds for the Central Universities [Grant No. HIT.NSRIF.2019073], and the Research Innovation Fund.

참고문헌

  1. Balabanova L, Slepchenko L, Son O, et al. Biotechnology potential of marine fungi degrading plant and algae polymeric substrates. Front Microbiol. 2018;9:1527. https://doi.org/10.3389/fmicb.2018.01527
  2. Xu LJ, Meng W, Cao C, et al. Antibacterial and antifungal compounds from marine fungi. Mar Drugs. 2015;13:3479-3513. https://doi.org/10.3390/md13063479
  3. Moghadamtousi SZ, Nikzad S, Kadir HA, et al. Potential antiviral agents from marine fungi: an overview. Mar Drugs. 2015;13:4520-4538. https://doi.org/10.3390/md13074520
  4. Han WB, Zhang AH, Deng XZ, et al. Curindolizine, an anti-inflammatory agent assembled via Michael addition of pyrrole alkaloids inside fungal cells. Org Lett. 2016;18:1816-1819. https://doi.org/10.1021/acs.orglett.6b00549
  5. Morita RY. Starvation survival of heterotrophs in the marine environment. Adv Microbial Ecol. 1982;6:171-198. https://doi.org/10.1007/978-1-4615-8318-9_5
  6. Roth FJ, Orpurt PA, Ahearn DJ. Occurrence and distribution of fungi in a subtropical marine environment. Can J Bot. 1964;42:375-383. https://doi.org/10.1139/b64-037
  7. Burgaud G, Calvez TL, Arzur D, et al. Diversity of culturable marine filamentous fungi from deep-sea hydrothermal vents. Environ Microbiol. 2009;11:1588-1600. https://doi.org/10.1111/j.1462-2920.2009.01886.x
  8. Nagano Y, Nagahama T, Hatada Y, et al. Fungal diversity in deep-sea sediments-the presence of novel fungal groups. Fungal Ecol. 2010;3:316-325. https://doi.org/10.1016/j.funeco.2010.01.002
  9. Edgcomb VP, Beaudoin D, Gast R, et al. Marine subsurface eukaryotes: the fungal majority. Environ Microbiol. 2011;13:172-183. https://doi.org/10.1111/j.1462-2920.2010.02318.x
  10. Lai X, Cao L, Tan H, et al. Fungal communities from methane hydrate-bearing deep-sea marine sediments in South China Sea. ISME J. 2007;1:756-762. https://doi.org/10.1038/ismej.2007.51
  11. Nagahama T, Takahashi E, Nagano Y, et al. Molecular evidence that deep-branching fungi are major fungal components in deep-sea methane cold-seep sediments. Environ Microbiol. 2011;13:2359-2370. https://doi.org/10.1111/j.1462-2920.2011.02507.x
  12. Singh P, Raghukumar C, Meena RM, et al. Fungal diversity in deep-sea sediments revealed by culture-dependent and culture-independent approaches. Fungal Ecol. 2012;5:543-553. https://doi.org/10.1016/j.funeco.2012.01.001
  13. Zhang XY, Wang GH, Xu XY, et al. Exploring fungal diversity in deep-sea sediments from Okinawa Trough using high-throughput Illumina sequencing. Deep-Sea Res. Part I. 2016;116:99-105. https://doi.org/10.1016/j.dsr.2016.08.004
  14. Zhang XY, Zhang Y, Xu XY, et al. Diverse deep-sea fungi from the South China Sea and their antimicrobial activity. Curr Microbiol. 2013;67:525-530. https://doi.org/10.1007/s00284-013-0394-6
  15. Picard KT. Coastal marine habitats harbor novel early-diverging fungal diversity. Fungal Ecol. 2017;25:1-13. https://doi.org/10.1016/j.funeco.2016.10.006
  16. Takami H, Inoue A, Fuji F, et al. Microbial flora in the deepest sea mud of the Mariana Trench. FEMS Microbiol Lett. 1997;152:279-285. https://doi.org/10.1111/j.1574-6968.1997.tb10440.x
  17. Raghukumar C, Raghukumar S, Sheelu G, et al. Buried in time: culturable fungi in a deep-sea sediment core from the Chagos Trench, Indian Ocean. Deep-Sea Res Part I. 2004;51:1759-1768. https://doi.org/10.1016/j.dsr.2004.08.002
  18. Damare S, Raghukumar C, Raghukumar S. Fungi in deep-sea sediments of the central Indian basin. Deep-Sea Res Part I. 2006;53:14-27. https://doi.org/10.1016/j.dsr.2005.09.005
  19. Singh P, Raghukumar C, Verma P, et al. Fungal community analysis in the deep-sea sediments of the Central Indian Basin by culture-independent approach. Microb Ecol. 2011;61:507-517. https://doi.org/10.1007/s00248-010-9765-8
  20. Thaler AD, Dover CLV, Vilgalys R. Ascomycete phylotypes recovered from a gulf of Mexico methane seep are identical to an uncultured deep-sea fungal clade from the Pacific. Fungal Ecol. 2012;5:270-273. https://doi.org/10.1016/j.funeco.2011.07.002
  21. Xu W, Luo ZH, Guo SS, et al. Fungal community analysis in the deep-sea sediments of the Pacific Ocean assessed by comparison of ITS, 18S and 28S ribosomal DNA regions. Deep-Sea Res Part I. 2016;109:51-60. https://doi.org/10.1016/j.dsr.2016.01.001
  22. Xu W, Pang KL, Luo ZH. High fungal diversity and abundance recovered in the deep-sea sediments of the Pacific Ocean. Microb Ecol. 2014;68:688-698. https://doi.org/10.1007/s00248-014-0448-8
  23. Ogaki MB, Coelho LC, Vieira R, et al. Cultivable fungi present in deep-sea sediments of Antarctica: taxonomy, diversity, and bioprospecting of bio-active compounds. Extremophiles. 2020;24:227-238. https://doi.org/10.1007/s00792-019-01148-x
  24. Singh P, Raghukumar C, Verma P, et al. Phylogenetic diversity of culturable fungi from the deep-sea sediments of the Central Indian Basin and their growth characteristics. Fungal Divers. 2010;40:89-102. https://doi.org/10.1007/s13225-009-0009-5
  25. Zain ME. Impact of mycotoxins on humans and animals. J Saudi Chem Soc. 2011;15:129-144. https://doi.org/10.1016/j.jscs.2010.06.006
  26. Cho KM, Math RK, Hong SY, et al. Iturin produced by Bacillus pumilus HY1 from Korean soybean sauce (Kanjang) inhibits growth of aflatoxin producing fungi. Food Control. 2009;20:402-406. https://doi.org/10.1016/j.foodcont.2008.07.010
  27. Kong Q, Shan S, Liu Q, et al. Biocontrol of Aspergillus flavus on peanut kernels by use of a strain of marine Bacillus megaterium. Int J Food Microbiol. 2010;139:31-35. https://doi.org/10.1016/j.ijfoodmicro.2010.01.036
  28. Zhou Y, Wang J, Gao X, et al. Isolation of a novel deep-sea Bacillus circulus strain and uniform design for optimization of its anti-aflatoxigenic bioactive metabolites production. Bioengineered. 2019;10:13-22. https://doi.org/10.1080/21655979.2019.1586055
  29. Park YC, Gunasekera SP, Lopez JV, et al. Metabolites from the marine-derived fungus Chromocleista sp. isolated from a deep-water sediment sample collected in the Gulf of Mexico. J Nat Prod. 2006;69:580-584. https://doi.org/10.1021/np058113p
  30. Daletos G, Ebrahim W, Ancheeva E, et al. Natural products from deep-sea-derived fungi - a new source of novel bioactive compounds? Curr Med Chem. 2018;25:186-207. https://doi.org/10.2174/0929867324666170314150121
  31. Wang YT, Xue YR, Liu CH. A brief review of bio-active metabolites derived from deep-sea fungi. Mar Drugs. 2015;13:4594-4616. https://doi.org/10.3390/md13084594
  32. Wang J, He W, Huang X, et al. Antifungal new oxepine-containing alkaloids and xanthones from the deep-sea-derived fungus Aspergillus versicolor SCSIO 05879. J Agric Food Chem. 2016;64:2910-2916. https://doi.org/10.1021/acs.jafc.6b00527
  33. Li X, Li XD, Li XM, et al. Wentinoids A-F, six new isopimarane diterpenoids from Aspergillus wentii SD-310, a deep-sea sediment derived fungus. RSC Adv. 2017;7:4387-4394. https://doi.org/10.1039/C6RA27209F
  34. Stoeck T, Epstein S. Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Appl Environ Microbiol. 2003;69:2657-2663. https://doi.org/10.1128/AEM.69.5.2657-2663.2003
  35. White TJ, Bruns TD, Lee SB, et al. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis N, Gelfand D, Sninsky J, et al. editors. PCR-protocols and applications - a laboratory manual. New York (NY): Academic; 1990.
  36. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673-4680. https://doi.org/10.1093/nar/22.22.4673
  37. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870-1874. https://doi.org/10.1093/molbev/msw054
  38. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406-425.
  39. Yan PS, Song Y, Sakuno E, et al. Cyclo(L-leucyl-L-prolyl) produced by Achromobacter xylosoxidans inhibits aflatoxin production by Aspergillus parasiticus. Appl Environ Microbiol. 2004;70:7466-7473. https://doi.org/10.1128/AEM.70.12.7466-7473.2004
  40. Jebaraj CS, Raghukumar C, Behnke A, et al. Fungal diversity in oxygen-depleted regions of the Arabian sea revealed by targeted environmental sequencing combined with cultivation. FEMS Microbiol Ecol. 2010;71:399-412. https://doi.org/10.1111/j.1574-6941.2009.00804.x
  41. Calvez TL, Burgaud G, Stephane M, et al. Fungal diversity in deep-sea hydrothermal ecosystems. Appl Environ Microb. 2009;75:6415-6421. https://doi.org/10.1128/AEM.00653-09
  42. Xu W, Guo S, Pang KL, et al. Fungi associated with chimney and sulfide samples from a South Mid-Atlantic Ridge hydrothermal site: distribution, diversity and abundance. Deep Sea Res Part I. 2017;123:48-55. https://doi.org/10.1016/j.dsr.2017.03.004
  43. Zhang X, Tang G, Xu X, et al. Insights into deep-sea sediment fungal communities from the East Indian Ocean using targeted environmental sequencing combined with traditional cultivation. PLoS One. 2014;9:e109118. https://doi.org/10.1371/journal.pone.0109118
  44. Shao Z, Sun F. Intracellular sequestration of manganese and phosphorus in a metal-resistant fungus Cladosporium cladosporioides from deep-sea sediment. Extremophiles. 2007;11:435-443. https://doi.org/10.1007/s00792-006-0051-0
  45. Takishita K, Tsuchiya M, Reimer JD, et al. Molecular evidence demonstrating the basidiomycetous fungus Cryptococcus curvatus is the dominant microbial eukaryote in sediment at the Kuroshima Knoll methane seep. Extremophiles. 2006;10:165-169. https://doi.org/10.1007/s00792-005-0495-7
  46. Bass D, Howe A, Brown N, et al. Yeast forms dominate fungal diversity in the deep oceans. Proc Biol Sci. 2007;274:3069-3077.
  47. Frisvad JC, Smedsgaard J, Larsen TO, et al. Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud Mycol. 2004;49:201-241.
  48. Nielsen JC, Grijseels S, Prigent S, et al. Global analysis of biosynthetic gene clusters reveals vast potential of secondary metabolite production in Penicillium species. Nat Microbiol. 2017;2:17044. https://doi.org/10.1038/nmicrobiol.2017.44
  49. Bai J, Zhang P, Bao G, et al. Imaging mass spectrometry-guided fast identification of antifungal secondary metabolites from Penicillium polonicum. Appl Microbiol Biotechnol. 2018;102:8493-8500. https://doi.org/10.1007/s00253-018-9218-8
  50. Park MS, Fong JJ, Oh SY, et al. Marine-derived Penicillium in Korea: diversity, enzyme activity, and antifungal properties. Antonie Van Leeuwenhoek. 2014;106:331-345. https://doi.org/10.1007/s10482-014-0205-5
  51. Huang S, Chen H, Li W, et al. Bioactive chaetoglobosins from the mangrove endophytic fungus Penicillium chrysogenum. Mar Drugs. 2016;14:172. https://doi.org/10.3390/md14100172
  52. Gao SS, Li XM, Li CS, et al. Penicisteroids a and b, antifungal and cytotoxic polyoxygenated steroids from the marine alga-derived endophytic fungus Penicillium chrysogenum QEN-24S. Bioorg Med Chem Lett. 2011;21:2894-2897. https://doi.org/10.1016/j.bmcl.2011.03.076
  53. Wang X, Radwan MM, Tarawneh AH, et al. Antifungal activity against plant pathogens of metabolites from the endophytic fungus Cladosporium cladosporioides. J Agric Food Chem. 2013;61:4551-4555. https://doi.org/10.1021/jf400212y
  54. Yue Y, Yu H, Li R, et al. Exploring the antibacterial and antifungal potential of jellyfish-associated marine fungi by cultivation-dependent approaches. PLoS One. 2015;10:e0144394. https://doi.org/10.1371/journal.pone.0144394
  55. Musetti R, Vecchione A, Stringher L, et al. Inhibition of sporulation and ultrastructural alterations of grapevine downy mildew by the endophytic fungus Alternaria alternata. Phytopathology. 2006;96:689-698. https://doi.org/10.1094/PHYTO-96-0689