Molecular Diversity of Fungi from Marine Oxygen-Deficient Environments (ODEs)

  • Cathrine Sumathi Jebaraj
  • Dominik Forster
  • Frank Kauff
  • Thorsten Stoeck
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 53)


Molecular diversity surveys of marine fungi have demonstrated that the species richness known to date is just the tip of the iceberg and that there is a large extent of unknown fungal diversity in marine habitats. Reports of novel fungal lineages at higher taxonomic levels are documented from a large number of marine habitats, including the various marine oxygen-deficient environments (ODEs). In the past few years, a strong focus of eukaryote diversity research has been on a variety of ODEs, as these environments are considered to harbor a large number of organisms, which are highly divergent to known diversity and could provide insights into the early eukaryotic evolution. ODEs that have been targeted so far include shallow water sediments, hydrothermal vent systems, deep-sea basins, intertidal habitats, and fjords. Most, if not all, molecular diversity studies in marine ODEs have shown, that contrary to previous assumptions, fungi contribute significantly to the micro-eukaryotic community in such habitats. In this chapter, we have reanalyzed the environmental fungal sequences obtained from the molecular diversity survey in 14 different sites to obtain a comprehensive picture of fungal diversity in these marine habitats. The phylogenetic analysis of the fungal environmental sequences from various ODEs have grouped these sequences into seven distinct clades (Clade 1–7) clustering with well-known fungal taxa. Apart from this, four environmental clades (EnvClade A, B, C, and D) with exclusive environmental sequences were also identified. This has provided information on the positioning of the environmental sequences at different taxonomic levels within the major fungal phylums. The taxonomic distribution of these environmental fungal sequences into clusters and clades has also shown that they are not restricted by geographical boundaries. The distribution pattern together with the reports on the respiratory abilities of fungi under reduced oxygen conditions shows that they are highly adaptive and may have a huge ecological role in these oxygen deficient habitats.


Terminal Restriction Fragment Length Polymorphism Fungal Diversity Fungal Taxon Environmental Sequence Fungal Sequence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This is NIO’s contribution no.4950.


  1. Alexander E, Stock A, Breiner HW, Behnke A, Bunge J, Yakimov MM, Stoeck T (2009) Microbial eukaryotes in the hypersaline anoxic L’Atalante deep-sea basin. Environ Microb 11:360–381CrossRefGoogle Scholar
  2. Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. Van Stockum & Zoon, The Hague, The NetherlandsGoogle Scholar
  3. Barghoorn ES, Linder DH (1944) Marine fungi: their taxonomy and biology. Farlowia 1:395–467Google Scholar
  4. Bass D, Howe A, Brown N, Barton H, Demidova M, Michelle H, Li L, Sanders H, Watkinson CV, Willcock S, Richards TA (2007) Yeast forms dominate fungal diversity in the deep oceans. Proc R Soc B 274:3069–3077PubMedCrossRefGoogle Scholar
  5. Behnke A, Bunge J, Barger K, Breiner HW, Alla V, Stoeck T (2006) Microeukaryote community patterns along an O2/H2S gradient in a supersulfidic anoxic fjord (Framvaren, Norway). Appl Environ Microbiol 72:626–3636CrossRefGoogle Scholar
  6. Bollag JM, Tung G (1972) Nitrous oxide release by soil fungi. Soil Biol Biochem 4:271–276CrossRefGoogle Scholar
  7. Bruns TD (2001) ITS reality. Inoculum 52:2–3Google Scholar
  8. Buchan A, Newell SY, Moreta JIJ, Moran MA (2002) Analysis of internal transcribed spacer (ITS) regions of rRNA genes in fungal communities in a southeastern U.S. salt marsh. Microb Ecol 43:329–340PubMedCrossRefGoogle Scholar
  9. Damare S, Raghukumar C, Raghukumar S (2006) Fungi in deep-sea sediments of the central Indian basin. Deep Sea Res I 53:14–27CrossRefGoogle Scholar
  10. Dawson SC, Pace NR (2002) Novel kingdom-level eukaryotic diversity in anoxic environments. Proc Natl Acad Sci U S A 99:8324–8329PubMedCrossRefGoogle Scholar
  11. Dighton J (2003) Fungi in ecosystem processes. Marcel Dekker, New YorkCrossRefGoogle Scholar
  12. Dighton J (2007) Nutrient cycling by saprotrophic fungi in terrestrial habitats. In: Kubicek CP, Druzhinina IS (eds) The Mycota IV, environmental and microbial relationships, 2nd edn. Springer, BerlinGoogle Scholar
  13. Edgcomb VP, Kysela DT, Teske A, de Vera GA, Sogin ML (2002) Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc Natl Acad Sci U S A 99:7658–7662PubMedCrossRefGoogle Scholar
  14. Edgcomb VP, Orsi W, Leslin C, Epstein S, Bunge J, Jeon SO et al (2009) Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the eastern Mediterranean Sea. Extremophiles 13:151–167PubMedCrossRefGoogle Scholar
  15. Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A (2011) Marine subsurface eukaryotes: the fungal majority. Environ Microbiol 13:172–183PubMedCrossRefGoogle Scholar
  16. Epstein S, López-García P (2007) ‘Missing’ protists: a molecular prospective. Biodivers Conserv 17:261–276CrossRefGoogle Scholar
  17. Fell JW, Boekhout T, Fonseca A, Sampaio JP (2001) Basidiomycetous yeasts. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) Mycota VII. Part B, Systematics and evolution. Springer, BerlinGoogle Scholar
  18. Gessner RV (1980) Degradative enzyme production by salt-marsh fungi. Bot Mar 23:133–139CrossRefGoogle Scholar
  19. Gleason FH, Schmidt SK, Marano AV (2010) Can zoosporic true fungi grow or survive in extreme or stressful environments? Extremophiles 14:417–425PubMedCrossRefGoogle Scholar
  20. Goregues CM, Michotey VD, Bonin PC (2005) Molecular, biochemical, and physiological approaches for understanding the ecology of denitrification. Mol Ecol 49:198–208Google Scholar
  21. Guarro J, Gene J, Stchigel AM (1999) Developments in fungal taxonomy. Clin Microbiol Rev 12:454–455PubMedGoogle Scholar
  22. Gunner HB, Alexander M (1964) Anaerobic growth of Fusarium oxysporum. J Bacteriol 37:1309–1315Google Scholar
  23. Hibbett DS, Binder M, Bischoff JF et al (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547PubMedCrossRefGoogle Scholar
  24. Hugenholtz P, Pace NR (1996) Identifying microbial diversity in the natural environment: a molecular phylogenetic approach. Trends Biotechnol 14:190–197PubMedCrossRefGoogle Scholar
  25. Hyde KD, Gareth Jones EB, Leana OE, Pointing SB, Poonyth AD, Vrijmoed LLP (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7:1147–1611CrossRefGoogle Scholar
  26. Jebaraj CS, Raghukumar C (2009) Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India. Mycol Res 113:100–109CrossRefGoogle Scholar
  27. 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 Microbiol Ecol 71:399–412PubMedCrossRefGoogle Scholar
  28. Jones EBG, Choeyklin R (2008) Ecology of marine and freshwater basidiomycetes. In: Boddy L, Franklan JC, West PV (eds) Ecology of saprotrophic basidiomycetes. Academic, New YorkGoogle Scholar
  29. Jones EBG, Hyde KD (2002) Succession: where to go from here? Fungal Divers 10:241–253Google Scholar
  30. Kagami M, de Bruin A, Ibelings BW, Donk EW (2007) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578:113–129CrossRefGoogle Scholar
  31. Kamykowski D, Zentara SJ (1990) Hypoxia in the world ocean as recorded in the historical data set. Deep Sea Res 37:1861–1874CrossRefGoogle Scholar
  32. Kerwin JL, Johnson LM, Whisler HC, Tuiniga AR (1992) Infection and morphogenesis of Pythium marinum in species of Porphyra and other red algae. Can J Bot 70:1017–1024CrossRefGoogle Scholar
  33. Kis-Papo T (2005) Marine fungal communities. In: Dighton J, White JF, Oudemans P (eds) The Fungal Community: its Organization and Role in the Ecosystem. Taylor & Francis, Boca Raton, FL, pp 61–92CrossRefGoogle Scholar
  34. Knowles R (1982) Denitrification. Microbiol Rev 46:43–70PubMedGoogle Scholar
  35. Kohlmeyer J, Kohlmeyer E (1979) Marine mycology. The higher fungi. Academic, New YorkGoogle Scholar
  36. Kurakov AV, Lavrent’ev RB, Nechitailo TY, Golyshin PN, Zvyagintsev DG (2008) Diversity of facultatively anaerobic microscopic mycelial fungi in soils. Microbiology 77:90–98CrossRefGoogle Scholar
  37. 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 1:756–762PubMedCrossRefGoogle Scholar
  38. Letcher PM, Powell MJ (2005) Kappamyces, a new genus in the Chytridiales (Chytridiomycota). Nova Hedwigia 80:113–133Google Scholar
  39. Levin LA (2003) Oxygen minimum zone benthos: adaptation and community response to hypoxia. In: Gibson RN, Atkinson RJ (eds) A oceanography and marine biology: an annual review. Taylor and Francis, New York, pp 1–45Google Scholar
  40. Le Calvez T, Burgaud G, MahÕ S, Barbier G, Vandenkoornhuyse P (2009) Fungal diversity in deep-sea hydrothermal ecosystems. Appl Environ Microbiol 75:6415–6421Google Scholar
  41. Lockhart RJ, van Dyke MI, Beadle IR, Humphreys P, McCarthy AJ (2006) Molecular detection of anaerobic gut fungi (Neocallimastigales) from landfill sites. Appl Environ Microbiol 72:5659–5661PubMedCrossRefGoogle Scholar
  42. López-García 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 U S A 100:697–702PubMedCrossRefGoogle Scholar
  43. López-García P, Vereshchaka A, Moreira D (2007) Eukaryotic diversity associated with carbonates and fluid-seawater interface in Lost City hydrothermal field. Environ Microbiol 9:546–554PubMedCrossRefGoogle Scholar
  44. Luo Q, Krumholz LR, Najar FZ, Peacock AD, Roe BA, White DC, Elshahed MS (2005) Diversity of the microeukaryotic community insulfide-rich Zodletone Spring (Oklahoma). Appl Environ Microbiol 71:6175–6184PubMedCrossRefGoogle Scholar
  45. Maheshwari R (2005) Species, their diversity and populations in fungi: experimental methods in biology. In: Maheshwari R (ed) Fungi experimental methods in biology, Mycology series 24. CRC, Boca Raton, FL, pp 191–205Google Scholar
  46. Maheshwari R, Bharadwaj G, Bhat MK (2000) Thermophilic fungi: their physiology and enzymes. Microbiol Mol Biol Rev 64:461–488PubMedCrossRefGoogle Scholar
  47. Malosso E, Waite IS, English L, Hopkins DW, O’Donnell AG (2006) Fungal diversity in maritime Antarctic soils determined using a combination of culture isolation, molecular fingerprinting and cloning techniques. Polar Biol 29:552–561CrossRefGoogle Scholar
  48. Miller WG, Padhye AA, Bonn W, Jensen E, Brandt ME, Ridgway SH (2002) Cryptococcosis in a bottlenose dolphin (Tursiops truncatus) caused by Cryptococcus neoformans var. gattii. J Clin Microbiol 40:721–724PubMedCrossRefGoogle Scholar
  49. Newell SY (1996) Established and potential impacts of eukaryotic mycelial decomposers in marine/terrestrial ecotones. J Exp Mar Biol Ecol 200:187–206CrossRefGoogle Scholar
  50. News Letter ISRO (2009) Discovery of new microorganisms in the stratosphere. Accessed 29 Nov 2010
  51. Nikolcheva L, Bärlocher F (2004) Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycol Prog 3:41–49CrossRefGoogle Scholar
  52. O’Brien HE, Parrent JL, Jackson JA, Moncalvo JM, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550PubMedCrossRefGoogle Scholar
  53. Pang KL, Mitchell JI (2005) Molecular approaches for assessing fungal diversity in marine substrata. Bot Mar 48:332–347CrossRefGoogle Scholar
  54. Prasannari K, Sridhar KR (2001) Diversity and abundance of higher marine fungi on woody substrates along the west coast of India. Curr Sci 81:304–311Google Scholar
  55. Raghukumar C, Raghukumar S, Sharma S, Chandramohan D (1992) Endolithic fungi from deep-sea calcareous substrata: isolation and laboratory studies. In: Desai BN (ed) Oceanography of the Indian Ocean. Oxford IBH Publication, New DelhiGoogle Scholar
  56. Raghukumar C, Raghukumar S, Sheelu G, Gupta SM, Nath B, Rao BR (2004) Buried in time: culturable fungi in a deep-sea sediment core from the Chagos Trench, Indian Ocean. Deep Sea Res I 51:1759–1768Google Scholar
  57. Roberts PL, Mitchell J, Jones EBG (1996) Morphological and taxonomical identification of marine ascomycetes: detection of races in geographical isolates of Corollospora maritima by RAPD analysis. In: Rossen L, Dawson MT, Frisvad J (ed.) Fungal identification techniques EU 16510 EN. European Commission, BruxellesGoogle Scholar
  58. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353CrossRefGoogle Scholar
  59. Sathe-Pathak V, Raghukumar S, Raghukumar C, Sharma S (1993) Thraustochytrid and fungal component of marine detritus. 1- Field studies on decomposition of the brown alga Sargassum cinereum. J Agr Indian J Mar Sci 22:159–167Google Scholar
  60. Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361PubMedCrossRefGoogle Scholar
  61. Shoun H, Kim DH, Uchiyama H, Sugiyama J (1992) Denitrification by fungi. FEMS Microbiol Lett 94:277–282CrossRefGoogle Scholar
  62. Slapeta J, Moreira D, Lopez-Garcıa P (2005) The extent of protist diversity: insights from molecular ecology of freshwater eukaryotes. Proc R Soc Lond [Biol] 272:2073–2081CrossRefGoogle Scholar
  63. Sparrow FK Jr (1936) Biological observations of the marine fungi of woods hole waters. Biol Bull 70:236–263CrossRefGoogle Scholar
  64. States JS, Christensen M (2001) fungi associated with biological soil crusts in desert grasslands of Utah and Wyoming. Mycologia 93:432–439CrossRefGoogle Scholar
  65. Stock A, Bunge J, Jurgens K, Stoeck T (2009) Protistan diversity in the suboxic and anoxic waters of the Gotland Deep (Baltic Sea) as revealed by 18S rRNA clone libraries. Aquat Microb Ecol 55:267–284CrossRefGoogle Scholar
  66. Stoeck T, Epstein S (2003) Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen depleted marine environments. Appl Environ Microbiol 69:2657–2663PubMedCrossRefGoogle Scholar
  67. Stoeck T, Taylor GT, Epstein SS (2003) Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea). Appl Environ Microbiol 69:5656–5663PubMedCrossRefGoogle Scholar
  68. Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS (2006) A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157:31–43PubMedCrossRefGoogle Scholar
  69. Stoeck T, Kasper J, Bunge J, Leslin C, Ilyin V, Epstein SS (2007a) Protistan diversity in the arctic: a case of paleoclimate shaping modern biodiversity? PLoS One 2:e728PubMedCrossRefGoogle Scholar
  70. Stoeck T, Zuendorf A, Breiner HW, Behnke A (2007b) A molecular approach to identify active microbes in environmental eukaryote clone libraries. Microb Ecol 53:328–339PubMedCrossRefGoogle Scholar
  71. Takishita K, Miyake H, Kawato M, Maruyama T (2005) Genetic diversity of microbial eukaryotes in anoxic sediment around fumaroles on a submarine caldera floor based on the small-subunit rDNA phylogeny. Extremophiles 9:185–196PubMedCrossRefGoogle Scholar
  72. Takishita K, Tsuchiyaa M, Kawatoa M, Ogurib K, Kitazatob H, Maruyamaa T (2007a) 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 158:51–64PubMedCrossRefGoogle Scholar
  73. Takishita K, Yubuki N, Kakizoe N, Inagaki Y, Maruyama T (2007b) 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 11:563–576PubMedCrossRefGoogle Scholar
  74. Turner BC, Perkins DD, Fairfield A (2001) Neurospora from natural populations: a global study. Fungal Genet Biol 32:67–92PubMedCrossRefGoogle Scholar
  75. Usuda K, Toritsuka N, Matsuo Y, Kim DH, Shoun H (1995) Denitrification by the fungus Cylindrocarpon tonkinense: anaerobic cell growth and two isozyme forms of cytochrome P-450nor. Appl Environ Microbiol 61:883–889PubMedGoogle Scholar
  76. van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998) Characterisation of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Mol Ecol 7:879–887PubMedCrossRefGoogle Scholar
  77. Wainwright M, Wickramasinghe NC, Narlikar JV, Rajaratnam P (2003) Microorganisms cultured from stratospheric air samples obtained at 41 km. FEMS Microbiol Lett 218:161–165PubMedCrossRefGoogle Scholar
  78. Wyrtki K (1962) The oxygen minima in relation to ocean circulation. Deep Sea Res 9:11–23Google Scholar
  79. Zack JC, Wildman HG (2004) Fungi in stressful environments. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi, inventory and monitoring methods. J Biol Chem 271:16263–16267Google Scholar
  80. Zhou Z, Takaya N, Nakamura A, Yamaguchi M, Takeo K, Shoun H (2002) Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi. J Biol Chem 277:1892–1896PubMedCrossRefGoogle Scholar
  81. Zuccaro A, Schulz B, Mitchell JI (2003) Molecular detection of ascomycetes associated with Fucus serratus. Mycol Res 107:451–466CrossRefGoogle Scholar
  82. Zuendorf A, Bunge J, Behnke A, Barger KJA, Stoeck T (2006) Diversity estimates of microeukaryotes below the chemocline of the anoxic Mariager Fjord, Denmark. Microb Ecol 58:476–491CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Cathrine Sumathi Jebaraj
    • 1
  • Dominik Forster
    • 2
  • Frank Kauff
    • 2
  • Thorsten Stoeck
    • 2
  1. 1.National Institute of Oceanography, Council of Scientific and Industrial ResearchDona PaulaIndia
  2. 2.Faculty of BiologyUniversity of KaiserslauternKaiserslauternGermany

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