Holden
James F.
Holden
James F.
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PreprintExperimental investigation on the controls of clumped isotopologue and hydrogen isotope ratios in microbial methane( 2018-06-14) Gruen, Danielle S. ; Wang, David T. ; Könneke, Martin ; Topçuoğlu, Begüm D ; Stewart, Lucy C. ; Goldhammer, Tobias ; Holden, James F. ; Hinrichs, Kai-Uwe ; Ono, ShuheiThe abundance of methane isotopologues with two rare isotopes (e.g., 13CH3D) has been proposed as a tool to estimate the temperature at which methane is formed or thermally equilibrated. It has been shown, however, that microbial methane from surface environments and from laboratory cultures is characterized by low 13CH3D abundance, corresponding to anomalously high apparent 13CH3D equilibrium temperatures. We carried out a series of batch culture experiments to investigate the origin of the non-equilibrium signals in microbial methane by exploring a range of metabolic pathways, growth temperatures, and hydrogen isotope compositions of the media. We found that thermophilic methanogens (Methanocaldococcus jannaschii, Methanothermococcus thermolithotrophicus, and Methanocaldococcus bathoardescens) grown on H2+CO2 at temperatures between 60 and 80°C produced methane with Δ13CH3D values (defined as the deviation from stochastic abundance) of 0.5 to 2.5‰, corresponding to apparent 13CH3D equilibrium temperatures of 200 to 600°C. Mesophilic methanogens (Methanosarcina barkeri and Methanosarcina mazei) grown on H2+CO2, acetate, or methanol produced methane with consistently low Δ13CH3D values, down to -5.2‰. Closed system effects can explain part of the non-equilibrium signals for methane from thermophilic methanogens. Experiments with M. barkeri using D-spiked water or D-labeled acetate (CD3COO-) indicate that 1.6 to 1.9 out of four H atoms in methane originate from water, but Δ13CH3D values of product methane only weakly correlate with the D/H ratio of medium water. Our experimental results demonstrate that low Δ13CH3D values are not specific to the metabolic pathways of methanogenesis, suggesting that they could be produced during enzymatic reactions common in the three methanogenic pathways, such as the reduction of methyl-coenzyme M. Nonetheless C-H bonds inherited from precursor methyl groups may also carry part of non-equilibrium signals.
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ArticleSulfide geochronology along the Endeavour Segment of the Juan de Fuca Ridge(John Wiley & Sons, 2013-07-08) Jamieson, John W. ; Hannington, Mark D. ; Clague, David A. ; Kelley, Deborah S. ; Delaney, John R. ; Holden, James F. ; Tivey, Margaret K. ; Kimpe, Linda E.Forty-nine hydrothermal sulfide-sulfate rock samples from the Endeavour Segment of the Juan de Fuca Ridge, northeastern Pacific Ocean, were dated by measuring the decay of 226Ra (half-life of 1600 years) in hydrothermal barite to provide a history of hydrothermal venting at the site over the past 6000 years. This dating method is effective for samples ranging in age from ∼200 to 20,000 years old and effectively bridges an age gap between shorter- and longer-lived U-series dating techniques for hydrothermal deposits. Results show that hydrothermal venting at the active High Rise, Sasquatch, and Main Endeavour fields began at least 850, 1450, and 2300 years ago, respectively. Barite ages of other inactive deposits on the axial valley floor are between ∼1200 and ∼2200 years old, indicating past widespread hydrothermal venting outside of the currently active vent fields. Samples from the half-graben on the eastern slope of the axial valley range in age from ∼1700 to ∼2925 years, and a single sample from outside the axial valley, near the westernmost valley fault scarp is ∼5850 ± 205 years old. The spatial relationship between hydrothermal venting and normal faulting suggests a temporal relationship, with progressive younging of sulfide deposits from the edges of the axial valley toward the center of the rift. These relationships are consistent with the inward migration of normal faulting toward the center of the valley over time and a minimum age of onset of hydrothermal activity in this region of 5850 years.
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ArticleBiogeochemical processes at hydrothermal vents : microbes and minerals, bioenergetics, and carbon fluxes(The Oceanography Society, 2012-03) Holden, James F. ; Breier, John A. ; Rogers, Karyn L. ; Schulte, Mitchell D. ; Toner, Brandy M.Hydrothermal vents are among the most biologically active regions of the deep ocean. However, our understanding of the limits of life in this extreme environment, the extent of biogeochemical transformation that occurs in the crust and overlying ocean, and the impact of vent life on regional and global ocean chemistry is in its infancy. Recently, scientific studies have expanded our view of how vent microbes gain metabolic energy at vents through their use of dissolved chemicals and minerals contained in ocean basalts, seafloor sulfide deposits, and hydrothermal plumes and, in turn, how they catalyze chemical and mineral transformations. The scale of vent environments and the difficulties inherent in the study of life above, on, and below the deep seafloor have led to the development of geochemical and bioenergetic models. These models predict habitability and biological activity based on the chemical composition of hydrothermal fluids, seawater, and the surrounding rock, balanced by the physiological energy demand of cells. This modeling, coupled with field sampling for ground truth and discovery, has led to a better understanding of how hydrothermal vents affect the ocean and global geochemical cycles, and how they influence our views of life on the early Earth and the search for life beyond our own planet.
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ArticleIntroduction to the special issue : From RIDGE to Ridge 2000(The Oceanography Society, 2012-03) Fornari, Daniel J. ; Beaulieu, Stace E. ; Holden, James F. ; Mullineaux, Lauren S. ; Tolstoy, MayaArticles in this special issue of Oceanography represent a compendium of research that spans the disciplinary and thematic breadth of the National Science Foundation's Ridge 2000 Program, as well as its geographic focal points. The mid-ocean ridge (MOR) crest is where much of Earth's volcanism is focused and where most submarine volcanic activity occurs. If we could look down from space at our planet with the ocean drained, the MOR's topography and shape, along with its intervening fracture zones, would resemble the seams on a baseball, with the ocean basins dominating our planetary panorama. The volcanic seafloor is hidden beneath the green-blue waters of the world's ocean, yet therein lie fundamental clues to how our planet works and has evolved over billions of years, something that was not clearly understood 65 years ago—witness the following quote from H.H. Hess (1962) in his essay on "geopoetry" and commentary on J.H.F. Umbgrove's (1947) comprehensive summary of Earth and ocean history: The birth of the oceans is a matter of conjecture, the subsequent history is obscure, and the present structure is just beginning to be understood. Fascinating speculation on these subjects has been plentiful, but not much of it predating the last decade [the 1950s] holds water.
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PreprintNonequilibrium clumped isotope signals in microbial methane( 2015-02-09) Wang, David T. ; Gruen, Danielle S. ; Lollar, Barbara Sherwood ; Hinrichs, Kai-Uwe ; Stewart, Lucy C. ; Holden, James F. ; Hristov, Alexander N. ; Pohlman, John W. ; Morrill, Penny L. ; Konneke, Martin ; Delwiche, Kyle B. ; Reeves, Eoghan P. ; Sutcliffe, Chelsea N. ; Ritter, Daniel J. ; Seewald, Jeffrey S. ; McIntosh, Jennifer C. ; Hemond, Harold F. ; Kubo, Michael D. Y. ; Cardace, Dawn ; Hoehler, Tori M. ; Ono, ShuheiMethane is a key component in the global carbon cycle with a wide range of anthropogenic and natural sources. Although isotopic compositions of methane have traditionally aided source identification, the abundance of its multiply-substituted “clumped” isotopologues, e.g., 13CH3D, has recently emerged as a proxy for determining methane-formation temperatures; however, the impact of biological processes on methane’s clumped isotopologue signature is poorly constrained. We show that methanogenesis proceeding at relatively high rates in cattle, surface environments, and laboratory cultures exerts kinetic control on 13CH3D abundances and results in anomalously elevated formation temperature estimates. We demonstrate quantitatively that H2 availability accounts for this effect. Clumped methane thermometry can therefore provide constraints on the generation of methane in diverse settings, including continental serpentinization sites and ancient, deep groundwaters.
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ArticleSeafloor 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.
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ArticleHydrogen 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.