Butterfield David A.

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David A.

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  • Article
    Diversity and distribution of subseafloor Thermococcales populations in diffuse hydrothermal vents at an active deep-sea volcano in the northeast Pacific Ocean
    (American Geophysical Union, 2006-12-20) Huber, Julie A. ; Butterfield, David A. ; Baross, John A.
    The presence, diversity, and distribution of a key group of subseafloor archaea, the Thermococcales, was examined in multiple diffuse flow hydrothermal vents at Axial Seamount, an active deep-sea volcano located in the northeast Pacific Ocean. A polymerase chain reaction (PCR) approach was used to determine if this group of subseafloor indicator organisms showed any phylogenetic distribution that may indicate distinct subseafloor communities at vents with different physical and chemical characteristics. Targeted primers for the Thermococcales 16S rRNA (small subunit ribosomal RNA) gene and intergenic transcribed spacer (ITS) region were designed and applied to organisms filtered in-situ directly from a variety of diffuse flow vents. Thermococcales were amplified from 9 of 11 samples examined, and it was determined that the ITS region is a better phylogenetic marker than the 16S rRNA in defining consistent groups of closely related sequences. Results show a relationship between environmental clone distribution and source vent chemistry. The most highly diluted vents with elevated iron and alkalinity contained a distinct group of Thermococcales as defined by the ITS region, suggesting separate subseafloor Thermococcales populations at diffuse vents within the Axial caldera.
  • Article
    Axial Seamount
    (Oceanography Society, 2010-03) Chadwick, William W. ; Butterfield, David A. ; Embley, Robert W. ; Tunnicliffe, Verena ; Huber, Julie A. ; Nooner, Scott L. ; Clague, David A.
    Axial Seamount is a hotspot volcano superimposed on the Juan de Fuca Ridge (JdFR) in the Northeast Pacific Ocean. Due to its robust magma supply, it rises ~ 800 m above the rest of JdFR and has a large elongate summit caldera with two rift zones that parallel and overlap with adjacent segments of the spreading center.
  • Article
    Multi-stage evolution of the Lost City hydrothermal vent fluids
    (Elsevier, 2022-08-13) Aquino, Karmina A. ; Früh-Green, Gretchen L. ; Rickli, Jörg ; Bernasconi, Stefano M. ; Lang, Susan Q. ; Lilley, Marvin D. ; Butterfield, David A.
    Serpentinization-influenced hydrothermal systems, such as the Lost City Hydrothermal Field (LCHF), are considered as potential sites for the origin of life. Despite an abundance of reducing power in this system (H2 and CH4), microbial habitability may be limited by high pH, elevated temperatures, and/or low concentrations of bioavailable carbon. At the LCHF, the relative contribution of biotic and abiotic processes to the vent fluid composition, especially in the lower temperature vents, remain poorly constrained. We present fluid chemistry and isotope data that suggest that all LCHF fluids are derived from a single endmember produced in the hotter, deeper subsurface essentially in the absence of microbial activity. The strontium isotope composition (87Sr/86Sr) of this fluid records the influence of underlying mantle and/or gabbroic rocks, whereas sulfur isotope composition indicates closed-system thermochemical sulfate reduction. Conductive cooling and transport is accompanied by continued sulfate reduction, likely microbial, and mixing with unaltered seawater, which produce second-order vents characterized by higher δ34Ssulfide and lower δ34Ssulfate values. Third-order vent fluids are produced by varying degrees of subsurface mixing between the first- and second-order fluids and a seawater-dominated fluid. Additional biotic and abiotic processes along different flow paths are needed to explain the spatial variability among the vents. Relationships between sulfur geochemistry and hydrogen concentrations dominantly reflect variations in temperature and/or distance from the primary outflow path. Methane concentrations are constant across the field which point to an origin independent of flow path and venting temperature. At Lost City, not all vent fluids appear to have zero Mg concentrations. Thus, we propose an extrapolation to a Sr isotope-endmember composition as an alternative method to estimate endmember fluid compositions at least in similar systems where a two-component mixing with respect to Sr isotopes between seawater and endmember fluids can be established.
  • Dataset
    Data collected from Miniature Autonomous Plume Recorders (MAPRs) deployed near the Axial Seamount on the Juan de Fuca Ridge on R/V Thomas G. Thompson TN327 in August 2015 and collected in July 2017.
    (Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2019-04-10) Baker, Edward T. ; Butterfield, David A.
    Data collected from Miniature Autonomous Plume Recorders (MAPRs) deployed near the Axial Seamount on the Juan de Fuca Ridge on R/V Thomas G. Thompson TN327 in August 2015 and collected in July 2017. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/731092
  • Article
    Metabolic strategies shared by basement residents of the lost city hydrothermal field
    (American Society for Microbiology, 2022-09-13) Brazelton, William J. ; McGonigle, Julia M. ; Motamedi, Shahrzad ; Pendleton, H. Lizethe ; Twing, Katrina I. ; Miller, Briggs C. ; Lowe, William J. ; Hoffman, Alessandrina M. ; Prator, Cecilia A. ; Chadwick, Grayson L. ; Anderson, Rika E. ; Thomas, Elaina ; Butterfield, David A. ; Aquino, Karmina A. ; Fruh-Green, Gretchen L. ; Schrenk, Matthew O. ; Lang, Susan Q.
    Alkaline fluids venting from chimneys of the Lost City hydrothermal field flow from a potentially vast microbial habitat within the seafloor where energy and organic molecules are released by chemical reactions within rocks uplifted from Earth’s mantle. In this study, we investigated hydrothermal fluids venting from Lost City chimneys as windows into subseafloor environments where the products of geochemical reactions, such as molecular hydrogen (H2), formate, and methane, may be the only available sources of energy for biological activity. Our deep sequencing of metagenomes and metatranscriptomes from these hydrothermal fluids revealed a few key species of archaea and bacteria that are likely to play critical roles in the subseafloor microbial ecosystem. We identified a population of Thermodesulfovibrionales (belonging to phylum Nitrospirota) as a prevalent sulfate-reducing bacterium that may be responsible for much of the consumption of H2 and sulfate in Lost City fluids. Metagenome-assembled genomes (MAGs) classified as Methanosarcinaceae and Candidatus Bipolaricaulota were also recovered from venting fluids and represent potential methanogenic and acetogenic members of the subseafloor ecosystem. These genomes share novel hydrogenases and formate dehydrogenase-like sequences that may be unique to hydrothermal environments where H2 and formate are much more abundant than carbon dioxide. The results of this study include multiple examples of metabolic strategies that appear to be advantageous in hydrothermal and subsurface alkaline environments where energy and carbon are provided by geochemical reactions.
  • Dataset
    DOC, POC, d13C-POC, PN from a diffuse vent in West Mata sampled in May 2009 using ROV Jason II deployed from R/V Thomas Thompson.
    (Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2021-04-15) Lin, Huei-Ting ; Butterfield, David A. ; Baker, Edward T. ; Resing, Joseph A. ; Huber, Julie ; Cowen, James
    DOC, POC, d13C-POC, PN from a diffuse vent in West Mata sampled in May 2009 using ROV Jason II deployed from R/V Thomas Thompson. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/844580
  • Preprint
    Precipitation and growth of barite within hydrothermal vent deposits from the Endeavour Segment, Juan de Fuca Ridge
    ( 2015-10) Jamieson, John W. ; Hannington, Mark D. ; Tivey, Margaret K. ; Hansteen, Thor ; Williamson, Nicole M.-B. ; Stewart, Margaret ; Fietzke, Jan ; Butterfield, David A. ; Frische, Matthias ; Allen, Leigh ; Cousens, Brian ; Langer, Julia
    Hydrothermal vent deposits form on the seafloor as a result of cooling and mixing of hot hydrothermal fluids with cold seawater. Amongst the major sulfide and sulfate minerals that are preserved at vent sites, barite (BaSO4) is unique because it requires the direct mixing of Ba-rich hydrothermal fluid with sulfate-rich seawater in order for precipitation to occur. Because of its extremely low solubility, barite crystals preserve geochemical fingerprints associated with conditions of formation. Here, we present data from petrographic and geochemical analyses of hydrothermal barite from the Endeavour Segment of the Juan de Fuca Ridge, northeast Pacific Ocean, in order to determine the physical and chemical conditions under which barite precipitates within seafloor hydrothermal vent systems. Petrographic analyses of 22 barite-rich samples show a range of barite crystal morphologies: dendritic and acicular barite forms near the exterior vent walls, whereas larger bladed and tabular crystals occur within the interior of chimneys. A two component mixing model based on Sr concentrations and 87Sr/86Sr of both seawater and hydrothermal fluid, combined with 87Sr/86Sr data from whole rock and laser-ablation ICP-MS analyses of barite crystals indicate that barite precipitates from mixtures containing as low as 17% and as high as 88% hydrothermal fluid component, relative to seawater. Geochemical modelling of the relationship between aqueous species concentrations and degree of fluid mixing indicates that Ba2+ availability is the dominant control on mineral saturation. Observations combined with model results support that dendritic barite forms from fluids of less than 40% hydrothermal component and with a saturation index greater than ~0.6, whereas more euhedral crystals form at lower levels of supersaturation associated with greater contributions of hydrothermal fluid. Fluid inclusions within barite indicate formation temperatures of between ~120 and 240°C during barite crystallization. The comparison of fluid inclusion formation temperatures to modelled mixing temperatures indicates that conductive cooling of the vent fluid accounts for 60 – 120°C reduction in fluid temperature. Strontium zonation within individual barite crystals records fluctuations in the amount of conductive cooling within chimney walls that may result from cyclical oscillations in hydrothermal fluid flux. Barite chemistry and morphology can be used as a reliable indicator for past conditions of mineralization within both extinct seafloor hydrothermal deposits and ancient land-based volcanogenic massive sulfide deposits.
  • Article
    Hydrogen limitation and syntrophic growth among natural assemblages of thermophilic methanogens at deep-sea hydrothermal vents
    (Frontiers Media, 2016-08-05) Topcuoglu, Begum D. ; Stewart, Lucy C. ; Morrison, Hilary G. ; Butterfield, David A. ; Huber, Julie A. ; Holden, James F.
    Thermophilic methanogens are common autotrophs at hydrothermal vents, but their growth constraints and dependence on H2 syntrophy in situ are poorly understood. Between 2012 and 2015, methanogens and H2-producing heterotrophs were detected by growth at 80∘C and 55∘C at most diffuse (7–40∘C) hydrothermal vent sites at Axial Seamount. Microcosm incubations of diffuse hydrothermal fluids at 80∘C and 55∘C demonstrated that growth of thermophilic and hyperthermophilic methanogens is primarily limited by H2 availability. Amendment of microcosms with NH4+ generally had no effect on CH4 production. However, annual variations in abundance and CH4 production were observed in relation to the eruption cycle of the seamount. Microcosm incubations of hydrothermal fluids at 80∘C and 55∘C supplemented with tryptone and no added H2 showed CH4 production indicating the capacity in situ for methanogenic H2 syntrophy. 16S rRNA genes were found in 80∘C microcosms from H2-producing archaea and H2-consuming methanogens, but not for any bacteria. In 55∘C microcosms, sequences were found from H2-producing bacteria and H2-consuming methanogens and sulfate-reducing bacteria. A co-culture of representative organisms showed that Thermococcus paralvinellae supported the syntrophic growth of Methanocaldococcus bathoardescens at 82∘C and Methanothermococcus sp. strain BW11 at 60∘C. The results demonstrate that modeling of subseafloor methanogenesis should focus primarily on H2 availability and temperature, and that thermophilic H2 syntrophy can support methanogenesis within natural microbial assemblages and may be an important energy source for thermophilic autotrophs in marine geothermal environments.
  • Preprint
    Isolated communities of Epsilonproteobacteria in hydrothermal vent fluids of the Mariana Arc seamounts
    ( 2010-05) Huber, Julie A. ; Cantin, Holly V. ; Huse, Susan M. ; Mark Welch, David B. ; Sogin, Mitchell L. ; Butterfield, David A.
    Low-temperature hydrothermal vent fluids represent access points to diverse microbial communities living in oceanic crust. This study examined the distribution, relative abundance, and diversity of Epsilonproteobacteria in 14 low-temperature vent fluids from 5 volcanically active seamounts of the Mariana Arc using a 454 tag sequencing approach. Most vent fluids were enriched in cell concentrations compared to background seawater, and quantitative PCR results indicated all fluids were dominated by bacteria. Operational taxonomic unit (OTU)-based statistical tools applied to 454 data show that all vents from the northern end of the Marian Arc grouped together, to the exclusion of southern arc seamounts, which were as distinct from one another as they were from northern seamounts. Statistical analysis also showed a significant relationship between seamount and individual vent groupings, suggesting that community membership may be linked to geographical isolation and not geochemical parameters. However, while there may be large-scale geographic differences, distance is not the distinguishing factor in microbial community composition. At the local scale, most vents host a distinct population of Epsilonprotoebacteria, regardless of seamount location. This suggests there may be barriers to exchange and dispersal for these vent endemic microorganisms at hydrothermal seamounts of the Mariana Arc.
  • Article
    Active subseafloor microbial communities from Mariana back-arc venting fluids share metabolic strategies across different thermal niches and taxa
    (Springer Nature, 2019-05-09) Trembath-Reichert, Elizabeth ; Butterfield, David A. ; Huber, Julie A.
    There are many unknowns regarding the distribution, activity, community composition, and metabolic repertoire of microbial communities in the subseafloor of deep-sea hydrothermal vents. Here we provide the first characterization of subseafloor microbial communities from venting fluids along the central Mariana back-arc basin (15.5–18°N), where the slow-spreading rate, depth, and variable geochemistry along the back-arc distinguish it from other spreading centers. Results indicated that diverse Epsilonbacteraeota were abundant across all sites, with a population of high temperature Aquificae restricted to the northern segment. This suggests that differences in subseafloor populations along the back-arc are associated with local geologic setting and resultant geochemistry. Metatranscriptomics coupled to stable isotope probing revealed bacterial carbon fixation linked to hydrogen oxidation, denitrification, and sulfide or thiosulfate oxidation at all sites, regardless of community composition. NanoSIMS (nanoscale secondary ion mass spectrometry) incubations at 80 °C show only a small portion of the microbial community took up bicarbonate, but those autotrophs had the highest overall rates of activity detected across all experiments. By comparison, acetate was more universally utilized to sustain growth, but within a smaller range of activity. Together, results indicate that microbial communities in venting fluids from the Mariana back-arc contain active subseafloor communities reflective of their local conditions with metabolisms commonly shared across geologically disparate spreading centers throughout the ocean.
  • Article
    Spatially distinct, temporally stable microbial populations mediate biogeochemical cycling at and below the seafloor in hydrothermal vent fluids
    (John Wiley & Sons, 2017-12-15) Fortunato, Caroline S. ; Larson, Benjamin I. ; Butterfield, David A. ; Huber, Julie A.
    At deep-sea hydrothermal vents, microbial communities thrive across geochemical gradients above, at, and below the seafloor. In this study, we determined the gene content and transcription patterns of microbial communities and specific populations to understand the taxonomy and metabolism both spatially and temporally across geochemically different diffuse fluid hydrothermal vents. Vent fluids were examined via metagenomic, metatranscriptomic, genomic binning, and geochemical analyses from Axial Seamount, an active submarine volcano on the Juan de Fuca Ridge in the NE Pacific Ocean, from 2013 to 2015 at three different vents: Anemone, Marker 33, and Marker 113. Results showed that individual vent sites maintained microbial communities and specific populations over time, but with spatially distinct taxonomic, metabolic potential, and gene transcription profiles. The geochemistry and physical structure of each vent both played important roles in shaping the dominant organisms and metabolisms present at each site. Genomic binning identified key populations of SUP05, Aquificales and methanogenic archaea carrying out important transformations of carbon, sulfur, hydrogen, and nitrogen, with groups that appear unique to individual sites. This work highlights the connection between microbial metabolic processes, fluid chemistry, and microbial population dynamics at and below the seafloor and increases understanding of the role of hydrothermal vent microbial communities in deep ocean biogeochemical cycles.
  • Article
    Seafloor incubation experiment with deep-sea hydrothermal vent fluid reveals effect of pressure and lag time on autotrophic microbial communities
    (American Society for Microbiology, 2021-04-13) Fortunato, Caroline S. ; Butterfield, David A. ; Larson, Benjamin I. ; Lawrence-Slavas, Noah ; Algar, Christopher K. ; Zeigler Allen, Lisa ; Holden, James F. ; Proskurowski, Giora ; Reddington, Emily ; Stewart, Lucy C. ; Topçuoğlu, Begüm D ; Vallino, Joseph J. ; Huber, Julie A.
    Depressurization and sample processing delays may impact the outcome of shipboard microbial incubations of samples collected from the deep sea. To address this knowledge gap, we developed a remotely operated vehicle (ROV)-powered incubator instrument to carry out and compare results from in situ and shipboard RNA stable isotope probing (RNA-SIP) experiments to identify the key chemolithoautotrophic microbes and metabolisms in diffuse, low-temperature venting fluids from Axial Seamount. All the incubations showed microbial uptake of labeled bicarbonate primarily by thermophilic autotrophic Epsilonbacteraeota that oxidized hydrogen coupled with nitrate reduction. However, the in situ seafloor incubations showed higher abundances of transcripts annotated for aerobic processes, suggesting that oxygen was lost from the hydrothermal fluid samples prior to shipboard analysis. Furthermore, transcripts for thermal stress proteins such as heat shock chaperones and proteases were significantly more abundant in the shipboard incubations, suggesting that depressurization induced thermal stress in the metabolically active microbes in these incubations. Together, the results indicate that while the autotrophic microbial communities in the shipboard and seafloor experiments behaved similarly, there were distinct differences that provide new insight into the activities of natural microbial assemblages under nearly native conditions in the ocean.
  • Article
    Organic biogeochemistry in West Mata, NE Kau hydrothermal vent fields
    (American Geophysical Union, 2021-03-17) Lin, Huei-Ting ; Butterfield, David A. ; Baker, Edward T. ; Resing, Joseph A. ; Huber, Julie A. ; Cowen, James P.
    The impact of submarine hydrothermal systems on organic carbon in the ocean—one of the largest fixed carbon reservoirs on Earth—could be profound. Yet, different vent sites show diverse fluid chemical compositions and the subsequent biological responses. Observations from various vent sites are to evaluate hydrothermal systems' impact on the ocean carbon cycle. A response cruise in May 2009 to an on-going submarine eruption at West Mata Volcano, northeast Lau Basin, provided an opportunity to quantify the organic matter production in a back-arc spreading hydrothermal system. Hydrothermal vent fluids contained elevated dissolved organic carbon, particulate organic carbon (POC), and particulate nitrogen (PN) relative to background seawater. The δ13C-POC values for suspended particles in the diffuse vent fluids (−15.5‰ and −12.3‰) are distinct from those in background seawater (−23 ± 1‰), indicative of unique carbon synthesis pathways of the vent microbes from the seawater counterparts. The first dissolved organic nitrogen concentrations reported for diffuse vents were similar to or higher than those for background seawater. Enhanced nitrogen fixation and denitrification removed 37%–89% of the total dissolved nitrogen in the recharging background seawater in the hydrothermal vent flow paths. The hydrothermal plume samples were enriched in POC and PN, indicating enhanced biological production. The total “dark” organic carbon production within the plume matches the thermodynamic prediction based on available reducing chemical substances supplied to the plume. This research combines the measured organic carbon contents with thermodynamic modeled results and demonstrates the importance of hydrothermal activities on the water column carbon production in the deep ocean.