Spatial distribution, diversity and composition of bacterial communities in sub-seafloor fluids at a deep-sea hydrothermal field of the Suiyo Seamount

Abstract Spatial distribution, diversity, and composition of bacterial communities within the shallow sub-seafloor at the deep-sea hydrothermal field of the Suiyo Seamount, Izu-Bonin Arc, Western Pacific Ocean, were investigated. Fluids were sampled from four boreholes in this area. Each borehole was located near or away from active vents, the distance ranging 2–40 m from active vents. In addition, fluids discharging from a natural vent and ambient seawater were sampled in this area. We extracted DNA from each sample, amplified bacterial 16S rRNA genes by PCR, cloned the PCR products and sequenced. The total number of clones analyzed was 348. Most of the detected phylotypes were affiliated with the phylum Proteobacteria, of which the detection frequency in each clone library ranged from 84.6% to 100%. The bacterial community diversity and composition were different between hydrothermal fluids and seawater, between fluids from the boreholes and the vent, and even among fluids from each borehole. The relative abundances of the phylotypes related to Thiomicrospira , Methylobacterium and Sphingomonas were significantly different among fluids from each borehole. The phylotypes related to Thiomicrospira and Alcanivorax were detected in all of the boreholes and vent samples. Our findings provide insights into bacterial communities in the shallow sub-seafloor environments at active deep-sea hydrothermal vent fields.

[1]  K. Timmis,et al.  Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. , 1998, International journal of systematic bacteriology.

[2]  K. Takai,et al.  Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. , 2008, FEMS microbiology ecology.

[3]  A. Ventosa,et al.  Methylobacterium hispanicum sp. nov. and Methylobacterium aquaticum sp. nov., isolated from drinking water. , 2005, International journal of systematic and evolutionary microbiology.

[4]  James R. Cole,et al.  The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis , 2004, Nucleic Acids Res..

[5]  J. Handelsman,et al.  Introducing DOTUR, a Computer Program for Defining Operational Taxonomic Units and Estimating Species Richness , 2005, Applied and Environmental Microbiology.

[6]  Akihiko Maruyama,et al.  Analysis of the archaeal sub-seafloor community at Suiyo Seamount on the Izu-Bonin Arc. , 2005, Advances in space research : the official journal of the Committee on Space Research.

[7]  K. Horikoshi,et al.  Distribution of Archaea in a Black Smoker Chimney Structure , 2001, Applied and Environmental Microbiology.

[8]  Y. Sako,et al.  Balnearium lithotrophicum gen. nov., sp. nov., a novel thermophilic, strictly anaerobic, hydrogen-oxidizing chemolithoautotroph isolated from a black smoker chimney in the Suiyo Seamount hydrothermal system. , 2003, International journal of systematic and evolutionary microbiology.

[9]  Yusuke Morimoto,et al.  Analysis of Dissimilatory Sulfite Reductase and 16S rRNA Gene Fragments from Deep-Sea Hydrothermal Sites of the Suiyo Seamount, Izu-Bonin Arc, Western Pacific , 2004, Applied and Environmental Microbiology.

[10]  K. Schleifer,et al.  ARB: a software environment for sequence data. , 2004, Nucleic acids research.

[11]  E. Stackebrandt,et al.  Nucleic acid techniques in bacterial systematics , 1991 .

[12]  J. Baross,et al.  A novel microbial habitat in the mid-ocean ridge subseafloor , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  F. Rodríguez-Valera,et al.  Genetic analysis of housekeeping genes reveals a deep-sea ecotype of Alteromonas macleodii in the Mediterranean Sea. , 2005, Environmental microbiology.

[14]  C. Vetriani,et al.  Mercury Adaptation among Bacteria from a Deep-Sea Hydrothermal Vent , 2005, Applied and Environmental Microbiology.

[15]  S. Giovannoni,et al.  Bacterial diversity among small-subunit rRNA gene clones and cellular isolates from the same seawater sample , 1997, Applied and environmental microbiology.

[16]  H. Wakita,et al.  Peculiar features of Suiyo Seamount hydrothermal fluids, Izu-Bonin Arc: Differences from subaerial volcanism , 1994 .

[17]  Keiko Kitamura,et al.  Microbial diversity in hydrothermal surface to subsurface environments of Suiyo Seamount, Izu-Bonin Arc, using a catheter-type in situ growth chamber. , 2004, FEMS Microbiology Ecology.

[18]  D. Lane 16S/23S rRNA sequencing , 1991 .

[19]  Stephen L. Rathbun,et al.  Quantitative Comparisons of 16S rRNA Gene Sequence Libraries from Environmental Samples , 2001, Applied and Environmental Microbiology.

[20]  H. Johnson,et al.  Microbial life in ridge flank crustal fluids. , 2006, Environmental microbiology.

[21]  A. Maruyama,et al.  Two Bacteria Phylotypes Are Predominant in the Suiyo Seamount Hydrothermal Plume , 2004, Applied and Environmental Microbiology.

[22]  K. Nealson,et al.  Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the epsilon-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. , 2004, International journal of systematic and evolutionary microbiology.

[23]  William A. Siebold,et al.  SAR11 clade dominates ocean surface bacterioplankton communities , 2002, Nature.

[24]  淑識 高野,et al.  水曜海山海底熱水系に産する熱水鉱物の産状と化学組成 : 海底設置型掘削装置によるアプローチ(地質, 海底熱水系における生物・地質の相互作用) , 2005 .

[25]  J. Fuhrman,et al.  Widespread Archaea and novel Bacteria from the deep sea as shown by 16S rRNA gene sequences , 1997 .

[26]  E. Delong,et al.  Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior , 2006, Science.

[27]  H. Harmsen,et al.  Distribution of microorganisms in deep-sea hydrothermal vent chimneys investigated by whole-cell hybridization and enrichment culture of thermophilic subpopulations , 1997, Applied and environmental microbiology.

[28]  Yohey Suzuki,et al.  Thiomicrospira thermophila sp. nov., a novel microaerobic, thermotolerant, sulfur-oxidizing chemolithomixotroph isolated from a deep-sea hydrothermal fumarole in the TOTO caldera, Mariana Arc, Western Pacific. , 2004, International journal of systematic and evolutionary microbiology.

[29]  S. Giovannoni,et al.  Detection of stratified microbial populations related to Chlorobium and Fibrobacter species in the Atlantic and Pacific oceans , 1996, Applied and environmental microbiology.

[30]  Satoshi Nakagawa,et al.  Aeropyrum camini sp. nov., a strictly aerobic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney. , 2004, International journal of systematic and evolutionary microbiology.

[31]  J. Baross,et al.  Temporal Changes in Archaeal Diversity and Chemistry in a Mid-Ocean Ridge Subseafloor Habitat , 2002, Applied and Environmental Microbiology.

[32]  Ken Takai,et al.  Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field , 2004, Extremophiles.

[33]  D. Karl The microbiology of deep-sea hydrothermal vents , 1995 .

[34]  Masataka Kinoshita,et al.  Recharge/discharge interface of a secondary hydrothermal circulation in the Suiyo Seamount of the Izu-Bonin arc, identified by submersible-operated heat flow measurements , 2006 .

[35]  J. Kuever,et al.  Distribution and Diversity of Sulfur-OxidizingThiomicrospira spp. at a Shallow-Water Hydrothermal Vent in the Aegean Sea (Milos, Greece) , 1999, Applied and Environmental Microbiology.

[36]  I. Good THE POPULATION FREQUENCIES OF SPECIES AND THE ESTIMATION OF POPULATION PARAMETERS , 1953 .

[37]  M Weizenegger,et al.  Bacterial phylogeny based on comparative sequence analysis (review) , 1998, Electrophoresis.

[38]  G. Muyzer,et al.  Increased species diversity and extended habitat range of sulfur-oxidizing Thiomicrospira spp , 1997, Applied and environmental microbiology.

[39]  Y. Takano,et al.  Mineralogy and Isotope Geochemistry of Active Submarine Hydrothermal Field at Suiyo Seamount, Izu–Bonin Arc, West Pacific Ocean , 2008 .

[40]  Y. Takano,et al.  Evidence of sub-vent biosphere: enzymatic activities in 308 °C deep-sea hydrothermal systems at Suiyo seamount, Izu–Bonin Arc, Western Pacific Ocean , 2005 .

[41]  D. Karl,et al.  Phylogenetic diversity of the bacterial community from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii , 1995, Applied and environmental microbiology.

[42]  Y. Sako,et al.  Persephonella hydrogeniphila sp. nov., a novel thermophilic, hydrogen-oxidizing bacterium from a deep-sea hydrothermal vent chimney. , 2003, International journal of systematic and evolutionary microbiology.

[43]  K. Horikoshi,et al.  Genetic diversity of archaea in deep-sea hydrothermal vent environments. , 1999, Genetics.

[44]  Yohey Suzuki,et al.  Geomicrobiological exploration and characterization of a novel deep-sea hydrothermal system at the TOTO caldera in the Mariana Volcanic Arc. , 2006, Environmental microbiology.

[45]  G. Muyzer,et al.  Phylogenetic relationships ofThiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments , 1995, Archives of Microbiology.

[46]  K. Horikoshi,et al.  Bacterial diversity in deep-sea sediments from different depths , 1999, Biodiversity & Conservation.

[47]  M. Kamekura,et al.  Thermococcus celericrescens sp. nov., a fast-growing and cell-fusing hyperthermophilic archaeon from a deep-sea hydrothermal vent. , 2007, International journal of systematic and evolutionary microbiology.

[48]  Akihiko Maruyama,et al.  Simultaneous Direct Counting of Total and Specific Microbial Cells in Seawater, Using a Deep-Sea Microbe as Target , 2000, Applied and Environmental Microbiology.

[49]  Y. Takano,et al.  Vertical distribution of amino acids and chiral ratios in deep sea hydrothermal sub-vents of the Suiyo Seamount, Izu-Bonin Arc, Pacific Ocean , 2004 .

[50]  Takeshi Naganuma,et al.  Distribution of Microorganisms in the Subsurface of the Manus Basin Hydrothermal Vent Field in Papua New Guinea , 2003, Applied and Environmental Microbiology.

[51]  J. Baross,et al.  Methane- and Sulfur-Metabolizing Microbial Communities Dominate the Lost City Hydrothermal Field Ecosystem , 2006, Applied and Environmental Microbiology.

[52]  R. S. Hanson,et al.  Methylobacterium, a New Genus of Facultatively Methylotrophic Bacteria , 1976 .

[53]  R. Prins,et al.  Oligotrophy and pelagic marine bacteria: Facts and fiction , 1997 .

[54]  A. Hiraishi,et al.  Phenotypic and genetic diversity of chlorine-resistant Methylobacterium strains isolated from various environments , 1995, Applied and environmental microbiology.

[55]  Deborah S. Kelley,et al.  Incidence and Diversity of Microorganisms within the Walls of an Active Deep-Sea Sulfide Chimney , 2003, Applied and Environmental Microbiology.

[56]  D. Prieur,et al.  Diversity of Bacteria and Archaea associated with a carbonate-rich metalliferous sediment sample from the Rainbow vent field on the Mid-Atlantic Ridge. , 2005, Environmental microbiology.

[57]  K. Nealson,et al.  Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. , 2003, International journal of systematic and evolutionary microbiology.

[58]  Ko-ichi Nakamura,et al.  Oceanithermus desulfurans sp. nov., a novel thermophilic, sulfur-reducing bacterium isolated from a sulfide chimney in Suiyo Seamount. , 2004, International journal of systematic and evolutionary microbiology.

[59]  K. Nealson,et al.  Deferribacter desulfuricans sp. nov., a novel sulfur-, nitrate- and arsenate-reducing thermophile isolated from a deep-sea hydrothermal vent. , 2003, International journal of systematic and evolutionary microbiology.

[60]  A. J. Jones,et al.  New Screening Software Shows that Most Recent Large 16S rRNA Gene Clone Libraries Contain Chimeras , 2006, Applied and Environmental Microbiology.

[61]  P. de Vos,et al.  Cultivation of Denitrifying Bacteria: Optimization of Isolation Conditions and Diversity Study , 2006, Applied and Environmental Microbiology.

[62]  Y. Sako,et al.  Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. , 2005, Environmental microbiology.

[63]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[64]  M. Sogin,et al.  Microbial Diversity of Hydrothermal Sediments in the Guaymas Basin: Evidence for Anaerobic Methanotrophic Communities , 2002, Applied and Environmental Microbiology.

[65]  J. Murrell,et al.  A novel pink-pigmented facultative methylotroph, Methylobacterium thiocyanatum sp. nov., capable of growth on thiocyanate or cyanate as sole nitrogen sources , 1998, Archives of Microbiology.

[66]  J. Baross,et al.  Thermophilic and hyperthermophilic microorganisms in 3–30°C hydrothermal fluids following a deep-sea volcanic eruption , 1998 .

[67]  Fabien Kenig,et al.  Fluids from Aging Ocean Crust That Support Microbial Life , 2003, Science.

[68]  Chenli Liu,et al.  Alcanivorax dieselolei sp. nov., a novel alkane-degrading bacterium isolated from sea water and deep-sea sediment. , 2005, International journal of systematic and evolutionary microbiology.

[69]  P. Golyshin,et al.  Microbial Community of a Hydrothermal Mud Vent Underneath the Deep-Sea Anoxic Brine Lake Urania (Eastern Mediterranean) , 2007, Origins of Life and Evolution of Biospheres.

[70]  Y. Sako,et al.  Marinithermus hydrothermalis gen. nov., sp. nov., a strictly aerobic, thermophilic bacterium from a deep-sea hydrothermal vent chimney. , 2003, International journal of systematic and evolutionary microbiology.

[71]  T. Gold,et al.  The deep, hot biosphere. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[72]  C. Moyer,et al.  Neutrophilic Fe-Oxidizing Bacteria Are Abundant at the Loihi Seamount Hydrothermal Vents and Play a Major Role in Fe Oxide Deposition , 2002, Applied and Environmental Microbiology.

[73]  K. Horikoshi,et al.  Culture-Dependent and -Independent Characterization of Microbial Communities Associated with a Shallow Submarine Hydrothermal System Occurring within a Coral Reef off Taketomi Island, Japan , 2007, Applied and Environmental Microbiology.

[74]  J. Baross,et al.  Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. , 2003, FEMS microbiology ecology.

[75]  E. Shock,et al.  Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. , 1997, Geochimica et cosmochimica acta.