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Fungi in Deep-Sea Ecosystems of the World Ocean: A Review

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Abstract

An analysis of data available in the literature on the taxonomic diversity, occurrence, abundance, and distribution of microscopic fungi in deep-sea pelagic and benthic habitats of the World Ocean is provided in this review. The homology of deep-sea species and those described from the terrestrial environment is of particular note. The adaptations that allow fungi to exist in extreme conditions of bottom sediments of the World Ocean are discussed.

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REFERENCES

  1. Borzykh, O.G. and Zvereva, L.V., The first data on deep-sea fungi from the Piip submarine volcano (Vulkanologov Massif, Bering Sea), Materialy 4-i Vserossiiskoi konferentsii molodykh uchenykh “Kompleksnye issledovaniya Mirovogo okeana” (Proc. Forth All-Russ. Conf. Young Sci. “Comprehensive Studies of the World Ocean”), Sevastopol: Morsk. Gidrofiz. Inst., 2019, pp. 209–210.

  2. Kafanov, A.I. and Kudryashov, V.A., Morskaya biogeografiya (Marine Biogeography), Moscow: Nauka, 2000.

  3. Abe, F., Piezophysiology of yeast: Occurrence and significance, Cell. Mol. Biol., 2004, vol. 50, no. 4, pp. 437–445.

    CAS  PubMed  Google Scholar 

  4. Arifeen, M.Z.U., Xue, Y.-R., and Liu, C.-H., Deep-sea fungi: Diversity, enzymes, and bioactive metabolites, in Fungi in Extreme Environments: Ecological Role and Biotechnological Significance, Cham: Springer, 2019, ch. 17, pp. 331–347.

    Google Scholar 

  5. Barone, G., Rastelli, E., Corinaldesi, C., et al., Benthic deep-sea fungi in submarine canyons of the Mediterranean Sea, Prog. Oceanogr., 2018, vol. 168, pp. 57–64. https://doi.org/10.1016/j.pocean.2018.09.011

    Article  Google Scholar 

  6. Bass, D., Howe, A., Brown, N., et al., Yeast forms dominate fungal diversity in the deep oceans, Proc. R. Soc. B, 2007, vol. 274, no. 1629, pp. 3069–3077.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bruun, A.F., The abyssal fauna: Its ecology, distribution and origin, Nature, 1956, vol. 177, no. 2, pp. 1105–1108.

    Article  Google Scholar 

  8. 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, vol. 25, no. 2, pp. 186–207. https://doi.org/10.2174/0929867324666170314150121

    Article  CAS  PubMed  Google Scholar 

  9. Damare, S. and Raghukumar, C., Fungi and macroaggregation in deep-sea sediments, Microb. Ecol., 2008, vol. 56, pp.168–177.

    Article  PubMed  Google Scholar 

  10. Damare, S., Raghukumar, C., and Raghukumar, S., Fungi in deep-sea sediments of the Central Indian Basin, Deep Sea Res., Part I, 2006, vol. 53, no. 1, pp. 14–27.

    Article  Google Scholar 

  11. Daniel, I., Oger, P., and Winter, R., Origins of life and biochemistry under high-pressure conditions, Chem. Soc. Rev., 2006, vol. 35, no. 10, pp. 858–875.

    Article  CAS  PubMed  Google Scholar 

  12. DeLong, E.F. and Pace, N.R., Environmental diversity of bacteria and archaea, Syst. Biol., 2001, vol. 50, no. 4, pp. 470–478.

    Article  CAS  PubMed  Google Scholar 

  13. DeLong, E.F. and Yayanos, A.A., Adaptation of the membrane lipids of a deep-sea bacterium to changes in hydrostatic pressure, Science, 1985, vol. 228, no. 4703, pp. 1101–1103.

    Article  CAS  PubMed  Google Scholar 

  14. Dupont, J., Magnin, S., Rousseau, F., et al., Molecular and ultrastructural characterization of two ascomycetes found on sunken wood off Vanuatu Islands in the deep Pacific Ocean, Mycol. Res., 2009, vol. 113, no. 12, pp. 1351–1364.

    Article  CAS  PubMed  Google Scholar 

  15. Edgcomb, V.P., Beaudoin, D., Gast, R., et al., Marine subsurface eukaryotes: The fungal majority, Environ. Microbiol., 2011, vol. 13, no. 1, pp. 172–183.

    Article  CAS  PubMed  Google Scholar 

  16. Edgcomb, V.P., Kysela, D.T., Teske, A., et al., Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment, Proc. Natl. Acad. Sci. U. S. A., 2002, vol. 99, no. 11, pp. 7658–7662.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Fell, J.W., Yeasts in marine environments, in Marine Fungi and Fungal-Like Organisms, Gareth Jones, E.B. and Pang, K.-L., Eds., Berlin: De Gruyter, 2012, ch. 6, pp. 91–102.

    Google Scholar 

  18. Feng, L., Song, Q., Jiang, Q, and Li, Z., The horizontal and vertical distribution of deep-sea sediments fungal community in the South China Sea, Front. Mar. Sci., 2021, no. 8, 592784. https://doi.org/10.3389/fmars.2021.592784

  19. Fungi in Extreme Environments: Ecological Role and Biotechnological Significance, Cham: Springer, 2019.

  20. Höhnk, W., Über den pilzlichen Befall kalkiger Hartteile von Meerestieren, Ber. Dtsch. Wiss. Komm. Meeresforsch., 1969, vol. 20, pp. 129–140.

    Google Scholar 

  21. Hyde, K.D., Jones, E.B.G., and Moss, S.T., Mycelial adhesion to surfaces, in The Biology of Marine Fungi, Moss, S.T., Ed., Cambridge: Cambridge Univ. Press, 1986, ch. 28, pp. 331–340.

    Google Scholar 

  22. Jannasch, H.W., Wirsen, C.O., and Winget, C.L., A bacteriological pressure-retaining deep-sea sampler and culture vessel, Deep-Sea Res. Oceanogr. Abstr., 1973, vol. 20, no. 7, pp. 663–664.

    Article  Google Scholar 

  23. Jørgensen, B.B. and Boetius, A., Feast and famine – microbial life in the deep-sea bed, Nat. Rev. Microbiol., 2007, vol. 5, pp. 770–781.

    Article  PubMed  CAS  Google Scholar 

  24. Kohlmeyer, J., Eine neuer Ascomycet auf Hydrozoen im Südatlantik, Ber. Dtsch. Bot. Ges., 1971, vol. 83, nos. 9–10, pp. 505–509.

    Google Scholar 

  25. Kohlmeyer, J., New genera and species of higher fungi from the deep sea (1615–5315 m), Rev. Mycol., 1977, vol. 41, pp. 189–206.

    Google Scholar 

  26. Kohlmeyer, J. and Kohlmeyer, E., Marine Mycology: The Higher Fungi, New York: Academic, 1979.

    Google Scholar 

  27. Kohlmeyer, J. and Volkmann-Kohlemyer, B., Halographis (Opegraphales), a new endolithic lichenoid from corals and snails, Can. J. Bot., 1988, vol. 66, no. 6, pp. 1138–1141.

    Article  Google Scholar 

  28. Kutty, S.N. and Philip, R., Marine yeasts—a review, Yeast, 2008, vol. 25, no. 7, pp. 465–483.

    Article  CAS  PubMed  Google Scholar 

  29. Li, L., Kato, C., and Horikoshi, K., Bacterial diversity in deep-sea sediments from different depths, Biodiversity Conserv., 1999, vol. 8, pp. 659–677.

    Article  Google Scholar 

  30. Lara, E., Moreira, D., and López-García, P., The environmental clade LKM11 and Rozella form the deepest branching clade of Fungi, Protist, 2010, vol. 161, no. 1, pp. 116–121.

    Article  CAS  PubMed  Google Scholar 

  31. López-García, P., Rodríguez-Valera, F., Pedrós-Alió, C., and Moreira, D., Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton, Nature, 2001, vol. 409, no. 6820, pp. 603–607.

    Article  PubMed  Google Scholar 

  32. Lorenz, R. and Molitoris, H.P., Cultivation of fungi under simulated deep-sea conditions, Mycol. Res., 1997, vol. 110, no. 11, pp. 1355–1365.

    Article  Google Scholar 

  33. Manohar, C.S. and Raghukumar, C., Fungal diversity from various marine habitats deduced through culture-independent studies, FEMS Microbiol. Lett., 2013, vol. 341, no. 2, pp. 69–78.

    Article  CAS  PubMed  Google Scholar 

  34. Marchese, P., Garzoli, L., Young, R., et al., Fungi populate deep-sea coral gardens as well as marine sediments in the Irish Atlantic Ocean, Environ. Microbiol., 2021, vol. 23, no. 8, pp. 4168–4184. https://doi.org/10.1111/1462-2920.15560

    Article  CAS  PubMed  Google Scholar 

  35. Munn, C.B., Marine Microbiology: Ecology and Applications, New York: Garland Science, 2011.

    Book  Google Scholar 

  36. Nagahama, T. and Nagano, Y., Cultured and uncultured fungal diversity in deep-sea environments, in Biology of Marine Fungi, Raghukumar, C., Ed., Berlin: Springer, 2012, vol. 53, pp. 173–187.

    Google Scholar 

  37. Nagahama, T., Hamamoto, M., Nakase, T., et al., Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean, Antonie van Leeuwenhoek, 2001, vol. 80, pp. 101–110.

    Article  CAS  PubMed  Google Scholar 

  38. Nagahama, T., Hamamoto, M., Nakase, T., and Horikoshi, K., Rhodotorula lamellibrachii sp. nov., a new yeast species from a tubeworm collected at the deep-sea floor in Sagami Bay and its phylogenetic analysis, Antonie van Leeuwenhoek, 2001, vol. 80, pp. 317–323.

    Article  CAS  PubMed  Google Scholar 

  39. Nagahama, T., Hamamoto, M., Nakase, T., and Horikoshi, K., Rhodotorula benthica sp. nov. and Rhodotorula calyptogenae sp. nov., novel yeast species from animals collected from the deep-sea floor, and Rhodotorula lysiniphila sp. nov., which is related phylogenetically, Int. J. Syst. Evol. Microbiol., 2003, vol. 53, no. 3, pp. 897–903.

    Article  CAS  PubMed  Google Scholar 

  40. Nagano, Y., Nagahama, T., Hatada, Y., et al., Fungal diversity in deep-sea sediments—The presence of novel fungal groups, Fungal Ecol., 2010, vol. 3, no. 4, pp. 316–325.

    Article  Google Scholar 

  41. Nagano, Y., Fujiwara, Y., Nishimoto, A., et al., Deep-sea endemic fungi? The discovery of Alisea longicolla from artificially immersed wood in deep sea off the Nansei Islands, Japan, Mycoscience, 2019, vol. 60, no. 4, pp. 228–231.

    Article  Google Scholar 

  42. Ogaki, M.B., Coelho, L.C., Vieira, R., et al., Cultivable fungi present in deep-sea sediments of Antarctica: Taxonomy, diversity, and bioprospecting of bioactive compounds, Extremophiles, 2020, vol. 24, no. 2, pp. 227–238. https://doi.org/10.1007/s00792-019-01148-x

    Article  CAS  PubMed  Google Scholar 

  43. Ogaki, M.B., Pinto, O.H.B., Vieira, R., et al., Fungi present in Antarctic deep-sea sediments assessed using DNA metabarcoding, Microb. Ecol., 2021, vol. 82, no. 1, pp. 157–164. https://doi.org/10.1007/s00248-020-01658-8

    Article  CAS  PubMed  Google Scholar 

  44. Poulicek, M., Machiroux, R., and Toussaint, C., Chitin diagenesis in deep-water sediments, in Chitin in Nature and Technology, New York: Plenum, 1986, pp. 523–530.

    Google Scholar 

  45. Raghukumar, S., Fungi in Coastal and Oceanic Marine Ecosystems: Marine Fungi, Cham: Springer, 2017.

    Book  Google Scholar 

  46. Raghukumar, C. and Raghukumar, S., Barotolerance of fungi isolated from deep-sea sediments of the Indian Ocean, Aquat. Microb. Ecol., 1998, vol. 15, pp. 153–163.

    Article  Google Scholar 

  47. Raghukumar, C., Raghukumar, S., Sharma, S., and Chandramohan, D., Endolithic fungi from deep sea calcareous substrata: Isolation and laboratory studies, in Oceanography of the Indian Ocean, Desai, B.N., Ed., New Delhi: Oxford and IBH, 1992, pp. 3–9.

    Google Scholar 

  48. Raghukumar, C., Damare, S.R., and Singh, P., A review on deep-sea fungi: Occurrence, diversity and adaptations, Bot. Mar., 2010, vol. 53, no. 6, pp. 479–492.

    Article  Google Scholar 

  49. 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, vol. 51, pp. 1759–1768.

    Article  CAS  Google Scholar 

  50. Rédou, V., Navarri, M., Meslet-Cladière, L., et al., Species richness and adaptation of marine fungi from deep-subseafloor sediments, Appl. Environ. Microbiol., 2015, vol. 81, no. 10, pp. 3571–3583.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Richards, T.A., Jones, M.D.M., Leonard, G., and Bass, D., Marine fungi: Their ecology and molecular diversity, Annu. Rev. Mar. Sci., 2012, vol. 4, pp. 495–522.

    Article  Google Scholar 

  52. Roth, F.J., Jr., Orpurt, P.A., and Ahearn, D.G., Occurrence and distribution of fungi in a subtropical marine environment, Can. J. Bot., 1964, vol. 42, no. 4, pp. 375–383.

    Article  Google Scholar 

  53. Siebenaller, J.F. and Somero, G.N., Biochemical adaptation to the deep sea, Rev. Aquat. Sci., 1989, no. 1, pp. 1–25.

  54. Simonato, F., Campanaro, S., Lauro, F.M., et al., Piezophilic adaptation: A genomic point of view, J. Biotechnol., 2006, vol. 126, no. 1, pp. 11–25.

    Article  CAS  PubMed  Google Scholar 

  55. Singh, P. and Raghukumar, C., Diversity and physiology of deep-sea yeasts: A review, Kavaka, 2014, vol. 43, pp. 50–63.

    Google Scholar 

  56. Singh, P., Raghukumar, C., Verma, P., and Shouche, Y., Phylogenetic diversity of culturable fungi from the deep-sea sediments of the Central Indian Basin and their growth characteristics, Fungal Diversity, 2010, vol. 40, pp. 89–102.

    Article  Google Scholar 

  57. Singh, P., Raghukumar, C., Verma, P., and Shouche, Y., Fungal community analysis in the deep-sea sediments of the Central Indian Basin by culture-independent approach, Microb. Ecol., 2011, vol. 61, no. 3, pp. 507–517.

    Article  CAS  PubMed  Google Scholar 

  58. Singh, P., Raghukumar, C., Meena, R.M., et al., Fungal diversity in deep-sea sediments revealed by culture-dependent and culture-independent approaches, Fungal Ecol., 2012, vol. 5, no. 5, pp. 543–553.

    Article  Google Scholar 

  59. Singh, P., Raghukumar, C., Verma, A.K., and Meena, R.M., Differentially expressed genes under simulated deep-sea conditions in the psychrotolerant yeast Cryptococcus sp. NIOCC#PY13, Extremophiles, 2012, vol. 16, pp. 777–785.

    Article  CAS  PubMed  Google Scholar 

  60. Singh, P., Raghukumar, C., Verma, P., and Shouche, Y., Assessment of fungal diversity in deep-sea sediments by multiple primer approach, World J. Microbiol. Biotechnol., 2012, vol. 28, pp. 659–667.

    Article  CAS  PubMed  Google Scholar 

  61. Sogin, M.L., Morrison, H.G., Huber, J.A., et al., Microbial diversity in the deep sea and the underexplored “rare biosphere”, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, no. 32, pp. 12115–12120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Somero, G.N., Adaptations to high hydrostatic pressure, Annu. Rev. Physiol., 1992, vol. 54, pp. 557–577.

    Article  CAS  PubMed  Google Scholar 

  63. Sverdrup, H.U., Johnson, M.W., and Fleming, R.H., The Oceans, Their Physics, Chemistry, and General Biology, New York: Prentice-Hall, 1942.

    Google Scholar 

  64. Takai, K. and Horikoshi, K., Genetic diversity of Archaea in deep-sea hydrothermal vent environments, Genetics, 1999, vol. 152, no. 4, pp. 1285–1297.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Takami, H., Isolation and characterization of microorganisms from deep-sea mud, in Extremophiles in Deep-Sea Environments, Horikoshi, K. and Tsujii, K., Eds., Tokyo: Springer, 1999, pp. 3–26.

    Google Scholar 

  66. Takishita, K., Tsuchiya, M., Reimer, J.D., and Maruyama, T., Molecular evidence demonstrating the basidiomycetous fungus Cryptococcus curvatus is the dominant microbial eukaryote in sediment at the Kuroshima Knoll methane seep, Extremophiles, 2006, vol. 10, pp. 165–169.

    Article  CAS  PubMed  Google Scholar 

  67. Wang, F.P., Lu, S.L., Orcutt, B.N., et al., Discovering the roles of subsurface microorganisms: Progress and future of deep biosphere investigation, Chin. Sci. Bull., 2013, vol. 58, pp. 456–467.

    Article  Google Scholar 

  68. Wang, Z.-P., Liu, Z.-Zh., Wang, Y.-L., et al., Fungal community analysis in seawater of the Mariana Trench as estimated by Illumina HiSeq, RSC Adv., 2019, vol. 9, no. 12, pp. 6956–6964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. West, A.J., Lin, C.-W., Lin, T.-C., et al., Mobilization and transport of coarse woody debris to the oceans triggered by an extreme tropical storm, Limnol. Oceanogr., 2011, vol. 56, no. 1, pp. 77–85.

    Article  Google Scholar 

  70. Xu, W., Pang, K.-L., and Luo, Z.-H., High fungal diversity and abundance recovered in the deep-sea sediments of the Pacific Ocean, Microb. Ecol., 2014, vol. 68, pp. 688–698.

    Article  CAS  PubMed  Google Scholar 

  71. Yamasato, K., Goto, S., Ohwada, K., et al., Yeasts from the Pacific Ocean, J. Gen. Appl. Microbiol., 1974, vol. 20, no. 5, pp. 289–307.

    Article  Google Scholar 

  72. Yanagibayashi, M., Nogi, Y., Li, L., and Kato, C., Changes in the microbial community in Japan Trench sediment from a depth of 6292 m during cultivation without decompression, FEMS Microbiol. Lett., 1999, vol. 170, no. 1, pp. 271–279.

    Article  CAS  PubMed  Google Scholar 

  73. Zhang, X.-Y., Tang, G.-L., Xu, X.-Y., 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, vol. 9, no. 10, e109118. https://doi.org/10.1371/journal.pone.0109118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Zhang, X., Li, Y., Yu, Z., et al., Phylogenetic diversity and bioactivity of culturable deep-sea-derived fungi from Okinawa Trough, J. Oceanol. Limnol., 2021, vol. 39, pp. 892–902.

    Article  Google Scholar 

  75. ZoBell, C.E. and Johnson, F.H., The influence of hydrostatic pressure on the growth and viability of terrestrial and marine bacteria, J. Bacteriol., 1949, vol. 57, no. 2, pp. 179–189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. ZoBell, C.E. and Morita, R.Y., Barophilic bacteria in some deep-sea sediments, J. Bacteriol., 1957, vol. 73, no. 4, pp. 563–568.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Zvereva, L.V., Borzykh, O.G. Fungi in Deep-Sea Ecosystems of the World Ocean: A Review. Russ J Mar Biol 48, 139–148 (2022). https://doi.org/10.1134/S1063074022030105

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