Abstract
The Kuroshima Knoll, located in the southern Ryukyu Arc, is known to actively bubble with gas containing methane and hydrogen sulfide from numerous fissures in the large carbonate pavement. Although ecological studies regarding macrobenthos and bacteria from Kuroshima Knoll have been intensively conducted, the community structure and ecological importance of microbial eukaryotes (protists) have not yet been investigated. In the present study, we directly extracted DNA from sediment of the Kuroshima Knoll at a depth of 640 m and constructed genetic libraries of PCR-amplified eukaryotic small-subunit ribosomal DNA (SSU rDNA). Although the SSU rDNA sequences of several types of benthic foraminifers were retrieved from the surface of the sediment, all other sequences (just below the sediment surface to approximately 9 cm below sediment surface) were derived from the basidiomycetous yeast Cryptococcus curvatus. Furthermore, sequences of the internal transcribed spacer of rDNA (ITS-rDNA) retrieved from the same sediment were identical to that of C. curvatus originating from terrestrial habitats. The diversity of microbial eukaryotes in the Kuroshima Knoll sediment seems to be extremely low and significantly different from that of other marine environments previously reported.
References
Alongi DM (1987) The distribution and composition of deep-sea microbenthos in a bathyal region of the western Coral Sea. Deep Sea Res 34:1245–1254
Alongi DM (1992) Bathymetric patterns of deep-sea benthic communities from bathyal to abyssal depths in the western South Pacific (Solomon and Coral Seas). Deep Sea Res 39:549–565
Berney C, Fahrni J, Pawlowski J (2004) How many novel eukaryotic ‘kingdoms’? Pitfalls and limitations of environmental DNA surveys. BMC Biol 2:13
Bernhard JM, Buck KR, Barry JP (2001) Monterey Bay cold-seep biota: assemblages, abundance, and ultrastructure of living foraminifera. Deep Sea Res I 48:2233–2249
Burnett BR (1981) Quantitative sampling of nanobiota (microbiota) of the deep-sea benthos-III. The bathyal San Diego trough. Deep Sea Res 28:649–663
Dromer F, Moulignier A, Dupont B, Gueho E, Baudrimont M, Improvisi L, Provost F, Gonzalez-Canali G (1995) Myeloradiculitis due to Cryptococcus curvatus in AIDS. AIDS 9:395–396
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
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Inagaki F, Tsunogai U, Suzuki M, Kosaka A, Machiyama H, Takai K, Nunoura T, Nealson KH, Horikoshi K (2004) Characterization of C1-metabolizing prokaryotic communities in methane seep habitats at the Kuroshima Knoll, southern Ryukyu Arc, by analyzing pmoA, mmoX, mxaF, mcrA, and 16S rRNA genes. Appl Environ Microbiol 70:7445–7455
Kohlmeyer J, Kohlmeyer E (1979) Yeast. In: Kohlmeyer J, Kohlmeyer E (eds) Marine mycology: the higher fungi. Academic, New York pp 556–606
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 USA 100:697–702
Machiyama H, Matsumoto T, Matsumoto R, Hattori M, Okano M, Iwase R, Tomaru H (2001) Outline of Shinkai 2000 dive surveys on the Kuroshima Knoll, off Ishigaki Island. JAMSTEC J Deep Sea Res 19:45–60
Moreira D, López-García P (2003) Are hydrothermal vents oases for parasitic protists? Trends Parasitol 19:556–558
Nagahama T, Hamamoto M, Nakase T, Horikoshi K (1999) Kluyveromyces nonfermentans sp. nov., a new yeast species isolated from the deep sea. Int J Syst Bacteriol 49:1899–1905
Nagahama T, Hamamoto M, Nakase T, Horikoshi K (2001a) 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 80:317–323
Nagahama T, Hamamoto M, Nakase T, Takami H, Horikoshi K (2001b) Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean. Antonie Van Leeuwenhoek 80:101–110
Nagahama T, Hamamoto M, Nakase T, Horikoshi K (2003a) 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 53:897–903
Nagahama T, Hamamoto M, Nakase T, Takaki Y, Horikoshi K (2003b) Cryptococcus surugaensis sp. nov., a novel yeast species from sediment collected on the deep-sea floor of Suruga Bay. Int J Syst Evol Microbiol 53:2095–2098
Nagahama T (2005) Yeast biodiversity in freshwater, marine and deep-sea environments. In: Rosa C, Peter G (eds) The yeast handbook—volume ‘Biodiversity and ecophysiology of Yeasts’. Springer, Berlin Heidelberg New York, pp 241–262
Pawlowski J, Bolivar I, Fahrni JF, Cavalier-Smith T, Gouy M (1996) Early origin of foraminifera suggested by SSU rRNA gene sequences. Mol Biol Evol 13:445–450
Rathburn AE, Perez ME, Martin JB, Day SA, Mahn C, Gieskes J, Ziebis W, Williams D, Bahls A (2003) Relationships between the distribution and stable isotopic composition of living benthic foraminifera and cold methane seep biogeochemistry in Monterey Bay, California. Geochem Geophys Geosyst 4:1–28
Robinson CA, Bernhard JM, Levin LA, Mendoza GF, Blanks JK (2004) Surficial hydrocarbon seep infauna from the lake ridge (Atlantic Ocean, 2150 m) and the Gulf of Mexico (690–2240 m). Mar Ecol 25:313–336
Rodríguez F, Oliver JL, Marín A, Medina JR (1990) The general stochastic model of nucleotide substitutions. J Theor Biol 142:485–501
Snider LJ, Burnett BR, Hessler RR (1984) The composition and distribution of meiofauna and nanobiota in a central North Pacific deep-sea area. Deep Sea Res 31:1225–1249
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 9:185–196
Acknowledgements
We thank Dr. M. Nishijima (NCIMB Japan) for useful information on yeast literature; Mr. M. Kawato (JAMSTEC) for technical assistance; the captain and crew of the R/V Natsushima and the commander, pilots and operation team of the ROV Hyper-Dolphin for dedicated efforts. This work was performed as part of the project ‘Study for Understanding of Function and Structure of the Marine Ecosystems in the Earth Systems’ conducted at JAMSTEC, and was supported in part by grants from the Japan Society for the Promotion of Science (No. 17770077 to K. Takishita).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by K. Horikoshi
Rights and permissions
About this article
Cite this article
Takishita, K., Tsuchiya, M., Reimer, J.D. et al. Molecular evidence demonstrating the basidiomycetous fungus Cryptococcus curvatus is the dominant microbial eukaryote in sediment at the Kuroshima Knoll methane seep. Extremophiles 10, 165–169 (2006). https://doi.org/10.1007/s00792-005-0495-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-005-0495-7