Person: Andrew W. Dale

Science Advances

Widespread energy limitation to life in global subseafloor sediments

Authors: James A. Bradley, Sandra Arndt, Jan P. Amend, Ewa Burwicz, Andrew W. Dale, M. Egger, Douglas E. LaRowe

Published: August 5, 2020

C-DEBI Contribution Number: 534

Abstract

Microbial cells buried in subseafloor sediments comprise a substantial portion of Earth’s biosphere and control global biogeochemical cycles; however, the rate at which they use energy (i.e., power) is virtually unknown. Here, we quantify organic matter degradation and calculate the power utilization of microbial cells throughout Earth’s Quaternary-age subseafloor sediments. Aerobic respiration, sulfate reduction, and methanogenesis mediate 6.9, 64.5, and 28.6% of global subseafloor organic matter degradation, respectively. The total power utilization of the subseafloor sediment biosphere is 37.3 gigawatts, less than 0.1% of the power produced in the marine photic zone. Aerobic heterotrophs use the largest share of global power (54.5%) with a median power utilization of 2.23 × 10⁻¹⁸ watts per cell, while sulfate reducers and methanogens use 1.08 × 10⁻¹⁹ and 1.50 × 10⁻²⁰ watts per cell, respectively. Most subseafloor cells subsist at energy fluxes lower than have previously been shown to support life, calling into question the power limit to life.

Source: http://dx.doi.org/10.1126/sciadv.aba0697

Publications > Journal Article

Geochimica et Cosmochimica Acta

Organic carbon and microbial activity in marine sediments on a global scale throughout the Quaternary

Authors: Douglas E. LaRowe, Sandra Arndt, James A. Bradley, Ewa Burwicz, Andrew W. Dale, Jan P. Amend

Published: July 28, 2020

C-DEBI Contribution Number: 538

Abstract

Microbial degradation of organic carbon in marine sediments is a key driver of global element cycles on multiple time scales. However, it is not known to what depth microorganisms alter organic carbon in marine sediments or how microbial rates of organic carbon processing change with depth, and thus time since burial, on a global scale. To better understand the connection between the dynamic carbon cycle and life’s limits in the deep subsurface, we have combined a number of global data sets with a reaction transport model (RTM) describing first, organic carbon degradation in marine sediments deposited throughout the Quaternary Period and second, a bioenergetic model for microbial activity. The RTM is applied globally, recognizing three distinct depositional environments – continental shelf, margin and abyssal zones. The results include the masses of particulate organic carbon, POC, stored in three sediment-depth layers: bioturbated Holocene (1.7 × 10¹⁷ g C), non-bioturbated Holocene (2.5 × 10¹⁸ g C) and Pleistocene (1.4 × 10²⁰ g C) sediments. The global depth-integrated rates of POC degradation have been determined to be 1.3 × 10¹⁵, 1.3 × 10¹⁴ and 3.0 × 10¹⁴ g C yr^-1 for the same three layers, respectively. A number of maps depicting the distribution of POC, as well as the fraction that has been degraded have also been generated. Using POC degradation as a proxy for microbial catabolic activity, total heterotrophic processing of POC throughout the Quaternary is estimated to be between 10^-11 – 10^-6 g C cm^-3 yr^-1, depending on the time since deposition and location. Bioenergetic modeling reveals that laboratory-determined microbial maintenance powers are poor predictors of sediment biomass concentration, but that cell concentrations in marine sediments can be accurately predicted by combining bioenergetic models with the rates of POC degradation determined in this study. Our model can be used to quantitatively describe both the carbon cycle and microbial activity on a global scale for marine sediments less than 2.59 million years old.

Source: http://dx.doi.org/10.1016/j.gca.2020.07.017

Publications > Journal Article

Geology

Temperature and volume of global marine sediments

Authors: Douglas E. LaRowe, Ewa Burwicz, Sandra Arndt, Andrew W. Dale, Jan P. Amend

Published: January 9, 2017

C-DEBI Contribution Number: 350

Abstract

Marine sediments contribute significantly to global element cycles on multiple time scales. This is due in large part to microbial activity in the shallower layers and abiotic reactions resulting from increasing temperatures and pressures at greater depths. Quantifying the rates of these diagenetic changes requires a three-dimensional description of the physiochemical properties of marine sediments. In a step toward reaching this goal, we have combined global data sets describing bathymetry, heat conduction, bottom-water temperatures, and sediment thickness to quantify the three-dimensional distribution of temperature in marine sediments. This model has revealed that ∼35% of sediments are above 60 °C, conditions that are suitable for petroleum generation. Furthermore, significant microbial activity could be inhibited in ∼25% of marine sediments, if 80 °C is taken as a major thermal barrier for subsurface life. In addition to a temperature model, we have calculated new values for the total volume (3.01 × 10⁸ km³) and average thickness (721 m) of marine sediments, and provide the only known determination of the volume of marine-sediment pore water (8.46 × 10⁷ km³), equivalent to ∼6.3% of the volume of the ocean. The results presented here can be used to help quantify the rates of mineral transformations, lithification, catagenesis, and the extent of life in the subsurface on a global scale.

Source: http://dx.doi.org/10.1130/g38601.1

Publications > Journal Article

Geochimica et Cosmochimica Acta

Sulfate reduction and methane oxidation activity below the sulfate-methane transition zone in Alaskan Beaufort Sea continental margin sediments: Implications for deep sulfur cycling

Authors: Tina Treude, Stefan Krause, Johanna Maltby, Andrew W. Dale, Richard B. Coffin, Leila J. Hamdan

Published: November 1, 2014

C-DEBI Contribution Number: 239

Abstract

Two ∼6 m long sediment cores were collected along the ∼300 m isobath on the Alaskan Beaufort Sea continental margin. Both cores showed distinct sulfate-methane transition zones (SMTZ) at 105 and 120 cm below seafloor (cmbsf). Sulfate was not completely depleted below the SMTZ but remained between 30 and 500 μM. Sulfate reduction and anaerobic oxidation of methane (AOM) determined by radiotracer incubations were active throughout the methanogenic zone. Although a mass balance could not explain the source of sulfate below the SMTZ, geochemical profiles and correlation network analyses of biotic and abiotic data suggest a cryptic sulfur cycle involving iron, manganese and barite. Inhibition experiments with molybdate and 2-bromoethanesulfonate (BES) indicated decoupling of sulfate reduction and AOM and competition between sulfate reducers and methanogens for substrates. While correlation network analyses predicted coupling of AOM to iron reduction, the addition of manganese or iron did not stimulate AOM. Since none of the classical archaeal anaerobic methanotrophs (ANME) were abundant, the involvement of unknown or unconventional phylotypes in AOM is conceivable. The resistance of AOM activity to inhibitors implies deviation from conventional enzymatic pathways. This work suggests that the classical redox cascade of electron acceptor utilization based on Gibbs energy yields does not always hold in diffusion-dominated systems, and instead biotic processes may be more strongly coupled to mineralogy.

Source: http://dx.doi.org/10.1016/j.gca.2014.08.018

Publications > Journal Article

Geochimica et Cosmochimica Acta

Thermodynamic limitations on microbially catalyzed reaction rates

Authors: Douglas E. LaRowe, Andrew W. Dale, Jan P. Amend, Philippe Van Cappellen

Published: August 1, 2012

C-DEBI Contribution Number: 222

Abstract

Quantification of global biogeochemical cycles requires knowledge of the rates at which microorganisms catalyze chemical reactions. In order for models that describe these processes to capture global patterns of change, the underlying formulations in them must account for biogeochemical transformations over seasonal and millennial time scales in environments characterized by different energy levels. Building on existing models, a new thermodynamic limiting function is introduced. With only one adjustable parameter, this function that can be used to model microbial metabolism throughout the range of conditions in which organisms are known to be active. The formulation is based on a comparison of the amount of energy available from any redox reaction to the energy required to maintain a membrane potential, a proxy for the minimum amount of energy required by an active microorganism. This function does not require species- or metabolism-specific parameters, and can be used to model metabolisms that capture any amount of energy. The utility of this new thermodynamic rate limiting term is illustrated by applying it to three low-energy processes: fermentation, methanogenesis and sulfate reduction. The model predicts that the rate of fermentation will be reduced by half once the Gibbs energy of the catalyzed reaction reaches −12 kJ (mol e⁻)⁻¹, and then slowing exponentially until the energy yield approaches zero. Similarly, the new model predicts that the low energy yield of methanogenesis, −4 to −0.5 kJ (mol e⁻)⁻¹, for a partial pressure of H₂ between 11 and 0.6 Pa decreases the reaction rate by 95–99%. Finally, the new function’s utility is illustrated through its ability to accurately model sulfate concentration data in an anoxic marine sediment.

Source: http://dx.doi.org/10.1016/j.gca.2012.05.011

Publications > Journal Article

Geochimica et Cosmochimica Acta

Modeling microbial reaction rates in a submarine hydrothermal vent chimney wall

Authors: Douglas E. LaRowe, Andrew W. Dale, David R. Aguilera, Ivan L’Heureux, Jan P. Amend, Pierre Regnier

Published: January 1, 2014

C-DEBI Contribution Number: 178

Abstract

The fluids emanating from active submarine hydrothermal vent chimneys provide a window into subseafloor processes and, through mixing with seawater, are responsible for steep thermal and compositional gradients that provide the energetic basis for diverse biological communities. Although several models have been developed to better understand the dynamic interplay of seawater, hydrothermal fluid, minerals and microorganisms inside chimney walls, none provide a fully integrated approach to quantifying the biogeochemistry of these hydrothermal systems. In an effort to remedy this, a fully coupled biogeochemical reaction-transport model of a hydrothermal vent chimney has been developed that explicitly quantifies the rates of microbial catalysis while taking into account geochemical processes such as fluid flow, solute transport and oxidation–reduction reactions associated with fluid mixing as a function of temperature. The metabolisms included in the reaction network are methanogenesis, aerobic oxidation of hydrogen, sulfide and methane and sulfate reduction by hydrogen and methane. Model results indicate that microbial catalysis is generally fastest in the hottest habitable portion of the vent chimney (77–102 °C), and methane and sulfide oxidation peak near the seawater-side of the chimney. The fastest metabolisms are aerobic oxidation of H₂ and sulfide and reduction of sulfate by H₂ with maximum rates of 140, 900 and 800 pmol cm⁻³ d⁻¹, respectively. The maximum rate of hydrogenotrophic methanogenesis is just under 0.03 pmol cm⁻³ d⁻¹, the slowest of the metabolisms considered. Due to thermodynamic inhibition, there is no anaerobic oxidation of methane by sulfate (AOM). These simulations are consistent with vent chimney metabolic activity inferred from phylogenetic data reported in the literature. The model developed here provides a quantitative approach to describing the rates of biogeochemical transformations in hydrothermal systems and can be used to constrain the role of microbial activity in the deep subsurface.

Source: http://dx.doi.org/10.1016/j.gca.2013.09.005

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Person: Andrew W. Dale

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