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High Fungal Diversity and Abundance Recovered in the Deep-Sea Sediments of the Pacific Ocean

  • Fungal Microbiology
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Abstract

Knowledge about the presence and ecological significance of bacteria and archaea in the deep-sea environments has been well recognized, but the eukaryotic microorganisms, such as fungi, have rarely been reported. The present study investigated the composition and abundance of fungal community in the deep-sea sediments of the Pacific Ocean. In this study, a total of 1,947 internal transcribed spacer (ITS) regions of fungal rRNA gene clones were recovered from five sediment samples at the Pacific Ocean (water depths ranging from 5,017 to 6,986 m) using three different PCR primer sets. There were 16, 17, and 15 different operational taxonomic units (OTUs) identified from fungal-universal, Ascomycota-, and Basidiomycota-specific clone libraries, respectively. Majority of the recovered sequences belonged to diverse phylotypes of Ascomycota (25 phylotypes) and Basidiomycota (18 phylotypes). The multiple primer approach totally recovered 27 phylotypes which showed low similarities (≤97 %) with available fungal sequences in the GenBank, suggesting possible new fungal taxa occurring in the deep-sea environments or belonging to taxa not represented in the GenBank. Our results also recovered high fungal LSU rRNA gene copy numbers (3.52 × 106 to 5.23 × 107copies/g wet sediment) from the Pacific Ocean sediment samples, suggesting that the fungi might be involved in important ecological functions in the deep-sea environments.

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References

  1. Alsumard LT, Golubic S, Priess K (1995) Fungi in corals: symbiosis or disease? Interactions between polyps and fungi cause pearl-like skeleton biomineralization. Mar Ecol Prog Ser 117:137–147

    Article  Google Scholar 

  2. Bass D, Howe A, Brown N, Barton H, Demidova M, Michelle H, Li L, Sander H, Watkinson SC, Willcock S, Richards TA (2007) Yeast forms dominate fungal diversity in the deep oceans. Proc Biol Sci 274:3069–3077

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Bates ST, Nash TH, Sweat KG, Garcia-Pichel F (2010) Fungal communities of lichen-dominated biological soil crusts: diversity, relative microbial biomass, and their relationship to disturbance and crust cover. J Arid Environ 74:1192–1199

    Article  Google Scholar 

  4. Burgaud G, Calvez TL, Arzur D, Vandenkoornhuyse P, Barbier G (2009) Diversity of culturable marine filamentous fungi from deep-sea hydrothermal vents. Environ Microbiol 11:1588–1600

    Article  PubMed  Google Scholar 

  5. Burgaud G, Arzur D, Durand L, Cambon-Bonavita MA, Barbier G (2010) Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna. FEMS Microb Ecol 73:121–133

    CAS  Google Scholar 

  6. Cocolin L, Manzano M, Aggio D, Cantoni C, Comi G (2001) A novel polymerase chain reaction (PCR)-denaturing gradient gel electrophoresis (DGGE) for the identification of Micrococcaceae strains involved in meat fermentations. Its application to naturally fermented Italian sausages. Meat Sci 58:59–64

    Article  CAS  PubMed  Google Scholar 

  7. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM (2004) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33:D294–D296

    Article  PubMed Central  Google Scholar 

  8. Connell L, Barrett A, Templeton A, Staudigel H (2009) Fungal diversity associated with an active deep sea volcano: Vailulu’u seamount, Samoa. Geomicrobiol J 26:597–605

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  10. Damare S, Raghukumar C, Raghukumar S (2006) Fungi in deep-sea sediments of the Central Indian Basin. Deep-Sea Res I 53:14–27

    Article  Google Scholar 

  11. Edgcomb VP, Kysela DT, Teske A, de Vera Gomez A, Sogin ML (2002) Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc Natl Acad Sci USA 99:7658–7662

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A (2011) Marine subsurface eukaryotes: the fungal majority. Environ Microbiol 13:172–183

    Article  CAS  PubMed  Google Scholar 

  13. Fell JW, Scorzetti G, Connell L, Craig S (2006) Biodiversity of micro-eukaryotes in Antarctic Dry Valley soils with 5 % soil moisture. Soil Biol Biochem 38:3107–3119

    Article  CAS  Google Scholar 

  14. Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Gadanho M, Sampaio JP (2005) Occurrence and diversity of yeasts in the mid-Atlantic ridge hydrothermal fields near the Azores Archipelago. Microb Ecol 50:408–417

    Article  CAS  PubMed  Google Scholar 

  16. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  17. Glud RN, Wenzhöfer F, Middelboe M, Oguri K, Turnewitsch R, Canfield DE, Kitazato H (2013) High rates of microbial carbon turnover in sediments in the deepest oceanic trench on Earth. Nat Geosci 6:284–288

    Article  CAS  Google Scholar 

  18. Hewitt EA, Muller KM, Cannone J, Hogan DJ, Gutell R, Prescott DM (2003) Phylogenetic relationships among 28 spirotrichous ciliates documented by rDNA. Mol Phylogenet Evol 29:258–267

    Article  CAS  PubMed  Google Scholar 

  19. Hyde KD, Jones EBG, Leano E, Pointing SB, Poonyth AD, Vrijmoed LLP (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7:1147–1161

    Article  Google Scholar 

  20. Jebaraj CS, Raghukumar C, Behnke A, Stoeck T (2010) Fungal diversity in oxygen-depleted regions of the Arabian Sea revealed by targeted environmental sequencing combined with cultivation. FEMS Microb Ecol 71:399–412

    Article  CAS  Google Scholar 

  21. Jones EBG, Sakayaroj J, Suetrong S, Somrithipol S, Pang KL (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:1–187

    Google Scholar 

  22. Kabir S, Rajendran N, Amemiya T, Itoh K (2003) Quantitative measurement of fungal DNA extracted by three different methods using real time polymerase chain reaction. J Biosci Bioeng 96:337–343

    Article  CAS  PubMed  Google Scholar 

  23. Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. Academic, New York

    Google Scholar 

  24. Kolb S, Knief C, Stubner S, Conrad R (2003) Quantitative detection of methanotrophs in soil by novel pmoA-targeted real-time PCR assays. Appl Environ Microbiol 69:2423–2429

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Lai X, Cao L, Tan H, Fang S, Huang Y, Zhou S (2007) Fungal communities from methane hydrate-bearing deep-sea marine sediments in South China Sea. ISME J 1:756–762

    Article  CAS  PubMed  Google Scholar 

  26. Le Calvez T, Burgaud G, Mahe S, Barbier G, Vandenkoornhuyse P (2009) Fungal diversity in deep sea hydrothermal ecosystems. Appl Environ Microbiol 75:6415–6421

    Article  PubMed Central  PubMed  Google Scholar 

  27. Lopez-Garcia P, Rodriguez-Valera F, Pedros-Alio C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607

    Article  CAS  PubMed  Google Scholar 

  28. Lopez-Garcia P, Philippe H, Gail F, Moreira D (2003) Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc Natl Acad Sci USA 100:697–702

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Lopez-Garcia P, Vereshchaka A, Moreira D (2007) Eukaryotic diversity associated with carbonates and fluid–seawater interface in Lost City hydrothermal field. Environ Microbiol 9:546–554

    Article  CAS  PubMed  Google Scholar 

  30. Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinforma 7:371

    Article  Google Scholar 

  31. Nagahama T, Nagano Y (2012) Cultured and uncultured fungal diversity in deep-sea environments. In: Raghukumar C (ed) Biology of marine fungi. Springer, Berlin, pp 173–187

    Chapter  Google Scholar 

  32. Nagahama T, Takahashi E, Nagano Y, Abdel-Wahab MA, Miyazaki M (2011) Molecular evidence that deep-branching fungi are major fungal components in deep-sea methane cold-seep sediments. Environ Microbiol 13:2359–2370

    Article  CAS  PubMed  Google Scholar 

  33. Nagano Y, Nagahama T, Hatada Y, Nunoura T, Takami H, Miyazaki J, Takai K, Horikoshi K (2010) Fungal diversity in deep-sea sediments—the presence of novel fungal groups. Fungal Ecol 3:316–325

    Article  Google Scholar 

  34. Nikolcheva LG, Bärlocher F (2004) Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycol Prog 3:41–49

    Article  Google Scholar 

  35. O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233

    Google Scholar 

  36. Pivkin MV (2000) Filamentous fungi associated with holothurians from the sea of Japan, off the primorye coast of Russia. Biol Bull 198:101–109

    Article  CAS  PubMed  Google Scholar 

  37. Raghukumar C (1986) Fungal parasites of the marine green alga Cladophora and Rhizoclonium. Bot Mar 29:289–297

    Article  Google Scholar 

  38. Renker C, Alphei J, Buscot F (2003) Soil nematodes associated with the mammal pathogenic fungal genus Malassezia (Basidiomycota: Ustilaginomycetes) in Central European forests. Biol Fertil Soils 37:70–72

    CAS  Google Scholar 

  39. Roth FJ, Orpurt PA, Ahearn DJ (1964) Occurrence and distribution of fungi in a subtropical marine environment. Can J Bot 42:375–383

    Article  Google Scholar 

  40. Sauvadet A-L, Gobet A, Guillou L (2010) Comparative analysis between protist communities from the deep-sea pelagic ecosystem and specific deep hydrothermal habitats. Environ Microbiol 12:2946–2964

    Article  CAS  PubMed  Google Scholar 

  41. Singh P, Raghukumar C, Verma P, Shouche Y (2010) Phylogenetic diversity of culturable fungi from the deep-sea sediments of the Central Indian Basin and their growth characteristics. Fungal Divers 40:89–102

    Article  Google Scholar 

  42. Singh P, Raghukumar C, Verma P, Shouche Y (2011) Fungal community analysis in the deep-sea sediments of the Central Indian Basin by culture-independent approach. Microb Ecol 61:507–517

    Article  CAS  PubMed  Google Scholar 

  43. Singh P, Raghukumar C, Verma P, Shouche Y (2012) Assessment of fungal diversity in deep-sea sediments by multiple primer approach. World J Microbiol Biotechnol 28:659–667

    Article  CAS  PubMed  Google Scholar 

  44. Smits THM, Devenoges C, Szynalski K, Maillard J, Holliger C (2004) Development of a real-time PCR method for quantification of the three genera Dehalobacter, Dehalococcoides, and Desulfitobacterium in microbial communities. J Microbiol Methods 57:369–378

    Article  CAS  PubMed  Google Scholar 

  45. Takishita K, Tsuchiya M, Kawato M, Oguri K, Kitazato H, Maruyama T (2007) Genetic diversity of microbial eukaryotes in anoxic sediment of the saline meromictic lake Namako-ike (Japan): on the detection of anaerobic or anoxic-tolerant lineages of eukaryotes. Protist 158:51–64

    Article  CAS  PubMed  Google Scholar 

  46. Takishita K, Yubuki N, Kakizoe N, Inagaki Y, Maruyama T (2007) Diversity of microbial eukaryotes in sediment at a deep-sea methane cold seep: surveys of ribosomal DNA libraries from raw sediment samples and two enrichment cultures. Extremophiles 11:563–576

    Article  CAS  PubMed  Google Scholar 

  47. Thaler AD, Dover CLV, Vilgalys R (2012) Ascomycete phylotypes recovered from a Gulf of Mexico methane seep are identical to an uncultured deep-sea fungal clade from the Pacific. Fungal Ecol 5:270–273

    Article  Google Scholar 

  48. White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, London, pp 315–322

    Google Scholar 

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Acknowledgments

This work was financially supported by the China Ocean Mineral Resources R&D Association (COMRA) Program (DY125-15-R-01) and National Natural Science Foundation of China (41376171). We thank the anonymous reviewers for their valuable comments on our manuscript.

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Authors and Affiliations

  1. School of Life Sciences, Xiamen University, Xiamen, 361005, People’s Republic of China

    Wei Xu

  2. Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, State Oceanic Administration, 178 Daxue Road, Xiamen, 361005, People’s Republic of China

    Wei Xu & Zhu-Hua Luo

  3. Collaborative Innovation Center for Development and Utilization of Marine Biological Resources, 178 Daxue Road, Xiamen, 361005, People’s Republic of China

    Wei Xu & Zhu-Hua Luo

  4. Institute of Marine Biology and Center of Excellence for the Oceans, National Taiwan Ocean University, 2 Pei-Ning Road, Keelung, 20224, Taiwan, Republic of China

    Ka-Lai Pang

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  1. Wei Xu
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Correspondence to Zhu-Hua Luo.

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Xu, W., Pang, KL. & Luo, ZH. High Fungal Diversity and Abundance Recovered in the Deep-Sea Sediments of the Pacific Ocean. Microb Ecol 68, 688–698 (2014). https://doi.org/10.1007/s00248-014-0448-8

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  • DOI: https://doi.org/10.1007/s00248-014-0448-8

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