Molecular evidence that phylogenetically diverged ciliates are active in microbial mats of deep-sea cold-seep sediment

Journal of Eukaryotic Microbiology

Volumn 57, Issue 1, 2010, Pages 76-86

  Takishita, Kiyotaka ^a   Kakizoe, Natsuki ^a,b   Yoshida, Takao ^a   Maruyama, Tadashi ^a  

^a JAPAN AGENCY FOR MARINE EARTH SCIENCE AND TECHNOLOGY   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Anaerobes; Biodiversity; Chemosynthetic ecosystem; Phylogeny; Protists; Ribosomal RNA

Indexed keywords

PROTOZOAL DNA; PROTOZOAL RNA; RIBOSOME DNA; RIBOSOME RNA; SEA WATER;

BIODIVERSITY; CHEMOSYNTHESIS; CILIATE; COLD SEEP; COMMUNITY STRUCTURE; DEEP SEA; DIVERGENCE; DNA; FUNGUS; METHANE; MICROBIAL MAT; MOLECULAR ANALYSIS; PHYLOGENETICS; PHYLOGENY; POLYMERASE CHAIN REACTION; PROKARYOTE; PROTIST; RNA;

ANIMAL; ARTICLE; BIODIVERSITY; CILIATE; CLASSIFICATION; COLD; CRYPTOCOCCUS; ECOSYSTEM; GENETICS; ISOLATION AND PURIFICATION; JAPAN; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEDIMENT;

ANIMALS; BIODIVERSITY; CILIOPHORA; COLD TEMPERATURE; CRYPTOCOCCUS; DNA, PROTOZOAN; DNA, RIBOSOMAL; ECOSYSTEM; EVOLUTION, MOLECULAR; GEOLOGIC SEDIMENTS; JAPAN; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, PROTOZOAN; RNA, RIBOSOMAL; SEAWATER; WATER MICROBIOLOGY;

HONSHU; JAPAN; KANTO; SAGAMI BAY;

ANIMALIA; ARCHAEA; BACTERIA (MICROORGANISMS); CILIOPHORA; CRYPTOCOCCUS CURVATUS; EUKARYOTA; FUNGI; PROKARYOTA; PROTISTA;

EID: 73349085213     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2009.00457.x     Document Type: Article

References (55)

1. Alexander, E., Stock, A., Breiner, H. W., Behnke, A., Bunge, J., Yakimov, M. M. Stoeck, T. 2009. Microbial eukaryotes in the hypersaline anoxic L'Atalante deep-sea basin. Environ. Microbiol., 11 : 360 381.
2. Bernard, C. Fenchel, T. 1996. Some microaerobic ciliates are facultative anaerobes. Eur. J. Protistol., 32 : 293 297.
3. Biagini, G. A., Finlay, B. J. Lloyd, D. 1998. Protozoan stimulation of anaerobic activity: enhancement of the rates of terminal decomposition of organic matter. FEMS Microbiol. Ecol., 27 : 1 8.
4. Boetius, A., Ravenschlag, K., Schubert, C. J., Rickert, D., Widdel, F., Gieseke, A., Amann, R., Jørgensen, B. B., Witte, U. Pfannkuche, O. 2000. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature, 407 : 623 626.
5. Coats, D. W. Park, M. G. 2002. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): parasite survival, infectivity, generation time, and host specificity. J. Phycol., 38 : 520 528.
6. Dyall, S. D., Brown, M. T. Johnson, P. J. 2004. Ancient invasions: from endosymbionts to organelles. Science, 304 : 253 257.
7. Edgcomb, V. P., Kysela, D. T., Teske, A., de Vera Gomez, A. Sogin, M. L. 2002. Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc. Natl. Acad. Sci. USA, 99 : 7658 7662.
8. Embley, T. M. Martin, W. 2006. Eukaryotic evolution, changes and challenges. Nature, 440 : 623 630.
9. Embley, T. M., van der Giezen, M., Horner, D. S., Dyal, P. L., Bell, S. Foster, P. G. 2003. Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life, 55 : 387 395.
10. Fang, J., Arakawa, S., Kato, C. Schouten, S. 2006. Microbial diversity of cold-seep sediments in Sagami Bay, Japan as determined by 16S rDNA and lipid analyses. FEMS Microbiol. Ecol., 57 : 429 441.
11. Fenchel, T. Finlay, B. J. 1995. Ecology and Evolution in Anoxic Worlds. Oxford University Press, Oxford.
12. Finlay, B. J. 1985. Nitrate respiration by protozoa (Loxodes spp.) in the hypolimnetic nitrate maximum of a productive freshwater pond. Freshwat. Biol., 15 : 333 346.
13. Finlay, B. J., Span, A. S. W. Harman, J. M. P. 1983. Nitrate respiration in primitive eukaryotes. Nature, 303 : 333 336.
14. Guillou, L., Viprey, M., Chambouvet, A., Welsh, R. M., Kirkham, A. R., Massana, R., Scanlan, D. J. Worden, A. Z. 2008. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ. Microbiol., 10 : 3349 3365.
15. Guindon, S. Gascuel, O. 2003. Simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol., 52 : 696 704.
16. Harada, A., Ohtsuka, S. Horiguchi, T. 2007. Species of the parasitic genus Duboscquella are members of the enigmatic Marine Alveolate Group I. Protist, 158 : 337 347.
17. Hashimoto, J., Ohta, S., Fujikura, K., Fujiwara, Y. Sukizaki, S. 1995. Life habit of vesicomyid clam, Calyptogena soyoae, and hydrogen sulfide concentration in interstitial waters in Sagami Bay, Japan. J. Oceanogr., 51 : 341 350.
18. Hugenholtzt, P. Huber, T. 2003. Chimeric 16S rDNA sequences of diverse origin are accumulating in the public databases. Int. J. Syst. Evol. Microbiol., 53 : 289 293.
19. Ikemoto, E. Kyo, M. 1993. Development of microbiological compact mud sampler. JAMSTEC Res., 30 : 1 16.
20. Inagaki, F., Sakihama, Y., Inoue, A., Kato, C. Horikoshi, K. 2002. Molecular phylogenetic analyses of reverse-transcribed bacterial rRNA obtained from deep-sea cold seep sediments. Environ. Microbiol., 4 : 277 286.
21. Inagaki, F., Tsunogai, U., Suzuki, M., Kosaka, A., Machiyama, H., Takai, K., Nunoura, T., Nealson, K. H. 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.
22. Keane, T. M., Naughton, T. J. McInerney, J. O. 2007. MultiPhyl: a high-throughput phylogenomics webserver using distributed computing. Nucl. Acids Res., 35 (Web Server Issue) : W33 W37.
23. Kemp, A. E. S., Pike, J., Pearce, R. B. Lange, C. B. 2000. The "Fall dump" - a new perspective on the role of a "shade flora" in the annual cycle of diatom production and export flux. Deep-Sea Res. II, 47 : 2129 2154.
24. Kennicutt, M. C. II., Brooks, J. M., Bidigare, R. R., Fay, R. R., Wade, T. L. McDonald, T. J. 1985. Vent-type taxa in a hydrocarbon seep region on the Louisianan slope. Nature, 317 : 351 353.
25. Kim, Y. W., Yasuda, M., Yamagishi, A., Oshima, T. Ohta, S. 1995. Characterization of the endosymbiont of a deep-sea bivalve, Calyptogena soyoae. Appl. Environ. Microbiol., 61 : 823 827.
26. Kobayashi, K. 2002. Tectonic significance of the cold seepage zones in the eastern Nankai accretionary wedge-an outcome of the 15 years' KAIKO projects. Mar. Geol., 187 : 3 30.
27. Li, L., Kato, C. Horikoshi, K. 1999. Microbial diversity in sediments collected from the deepest cold-seep area, the Japan Trench. Mar. Biotechnol., 1 : 391 400.
28. 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 : 546 554.
29. 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. (Pubitemid 36126115)
30. Lorenz, M. G. Wackernagel, G. 1987. Adsorption of DNA to sand and variable degradation rates of adsorbed DNA. Appl. Environ. Microbiol., 67 : 2354 2359.
31. Lynn, D. H. 2008. The Ciliated Protozoa. Characterization, Classification, and Guide to the Literature. Springer, London.
32. Maidak, B. L., Cole, J. R., Lilburn, T. G., Parker, C. T. Jr., Saxman, P. R., Farris, R. J., Garrity, G. M., Olsen, G. J., Schmidt, T. M. Tiedje, J. M. 2001. The RDP-II (Ribosomal Database Project). Nucl. Acids Res., 29 : 173 174.
33. Masuzawa, T., Handa, N., Kitagawa, H. Kusakabe, M. 1992. Sulfate reduction using methane in sediments beneath a bathyal 'cold seep' giant clam community off Hatsushima Island, Sagami Bay, Japan. Earth Planet Sci. Lett., 110 : 39 50.
34. Mayer, L. A., Shor, A. N., Hughes, J. Piper, D. J. W. 1988. Dense biological communities at 3,850 m on the Laurentian Fan and their relationship to the deposits of the 1929 Grand Banks earthquake. Deep-Sea Res., 35 : 1235 1246.
35. Miskin, I. P., Farrimond, P. Head, I. M. 1999. Identification of novel lineages as active members of microbial populations in a freshwater sediment using a rapid RNA extraction procedure and RT-PCR. Microbiology, 145 : 1977 1987.
36. Müller, M. 1993. The hydrogenosome. J. Gen. Microbiol., 139 : 2879 2889.
37. Nogales, B., Moore, E. R. B., Llobet-Brossa, E., Rossello-Mora, R., Amann, R. Timmis, K. N. 2001. Combined use of 16S ribosomal DNA and 16S rRNA to study the bacterial community of polychlorinated biphenyl-polluted soil. Appl. Environ. Microbiol., 67 : 1874 1884.
38. Nomura, M., Gourse, R. Baughman, G. 1984. Regulation of the synthesis of ribosomes and ribosomal components. Annu. Rev. Biochem., 53 : 75 117.
39. Ohta, S., Sakai, H., Taira, A., Ohwada, K., Ishii, T., Maeda, M., Fujioka, K., Saino, T., Kogure, K., Gamo, T., Shirayama, Y., Furuta, T., Ishizuka, T., Endow, K., Sumi, T., Hotta, H., Hashimoto, J., Handa, N., Masuzawa, T. Horikoshi, M. 1987. Multidisciplinary investigation of the Calyptogena communities at the Hatsushima site, Sagami Bay, central Japan. JAMSTEC Rep., 3 : 51 60.
40. Paull, C. K., Hecker, B., Commeau, R., Freeman-Lynde, R. P., Neumann, C., Corso, W. P., Golubic, S., Hook, J. E. Curray, J. 1984. Biological communities at the Florida escarpment resemble hydrothermal vent taxa. Science, 226 : 965 967.
41. Rinke, C., Schmitz-Esser, S., Stoecker, K., Nussbaumer, A. D., Molnár, D. A., Vanura, K., Wagner, M., Horn, M., Ott, J. A. Bright, M. 2006. Candidatus Thiobios zoothamnicoli," an ectosymbiotic bacterium covering the giant marine ciliate Zoothamnium niveum. Appl. Environ. Microbiol., 72 : 2014 2021.
42. Rodríguez, F., Oliver, J. L., Marin, A. Medina, J. R. 1990. The general stochastic model of nucleotide substitution. J. Theoret. Biol., 142 : 485 501.
43. Searcy, D. G. 2006. Rapid hydrogen sulfide consumption by Tetrahymena pyriformis and its implications for the origin of mitochondria. Eur. J. Protistol., 42 : 221 231.
44. Sibuet, M., Juniper, S. K. Pautot, G. 1988. Cold-seep benthic communities in the Japan subduction zones: geological control of community development. J. Mar. Res., 46 : 333 348.
45. Stamatakis, A., Hoover, P. Rougemont, J. 2008. A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol., 57 : 758 771.
46. Stoeck, T., Zuendorf, A., Breiner, H. W. Behnke, A. 2007. A molecular approach to identify active microbes in environmental eukaryote clone libraries. Microb. Ecol., 53 : 328 339.
47. Stoeck, T., Hayward, B., Taylor, G. T., Varela, R. Epstein, S. S. 2006. A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist, 157 : 31 43.
48. 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.
49. Takishita, K., Tsuchiya, M., Reimer, J. D. Maruyama, T. 2006. 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.
50. Takishita, K., Yubuki, N., Kakizoe, N., Inagaki, Y. Maruyama, T. 2007a. 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.
51. Takishita, K., Tsuchiya, M., Kawato, M., Oguri, K., Kitazato, H. Maruyama, T. 2007b. 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.
52. Thompson, J. D., Higgins, D. G. Gibson, T. J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res., 22 : 4673 4680.
53. Weller, R., Weller, J. W. Ward, D. M. 1991. 16S rRNA sequences of uncultivated hot spring cyanobacterial mat inhabitants retrieved as randomly primed cDNA. Appl. Environ. Microbiol., 57 : 1146 1151.
54. Werne, J. P., Baas, M. Sinninghe Damsté, J. S. 2002. Molecular isotopic tracing of carbon flow and trophic relationships in a methane-supported microbial community. Limnol. Oceanogr., 47 : 1694 1701.
55. Zuendorf, A., Bunge, J., Behnke, A., Barger, K. J. Stoeck, T. 2006. Diversity estimates of microeukaryotes below the chemocline of the anoxic Mariager Fjord, Denmark. FEMS Microbiol. Ecol., 58 : 476 491.