Geobiology (2014), 12, 172–181
DOI: 10.1111/gbi.12077
An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments N. RIEDINGER,1 M. J. FORMOLO,2 T. W. LYONS,1 S. HENKEL,3,* A. BECK4 AND S. KASTEN3,5 1
Department of Earth Sciences, University of California, Riverside, CA, USA Department of Geosciences, The University of Tulsa, Tulsa, OK, USA 3 Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany 4 Center for Geomicrobiology, Aarhus University, Aarhus C, Denmark 5 MARUM - Center for Marine Environmental Sciences and Department of Geosciences, University of Bremen, Bremen, Germany 2
ABSTRACT Here, we present results from sediments collected in the Argentine Basin, a non-steady state depositional marine system characterized by abundant oxidized iron within methane-rich layers due to sediment reworking followed by rapid deposition. Our comprehensive inorganic data set shows that iron reduction in these sulfate and sulfide-depleted sediments is best explained by a microbially mediated process—implicating anaerobic oxidation of methane coupled to iron reduction (Fe-AOM) as the most likely major mechanism. Although important in many modern marine environments, iron-driven AOM may not consume similar amounts of methane compared with sulfate-dependent AOM. Nevertheless, it may have broad impact on the deep biosphere and dominate both iron and methane cycling in sulfate-lean marine settings. Fe-AOM might have been particularly relevant in the Archean ocean, >2.5 billion years ago, known for its production and accumulation of iron oxides (in iron formations) in a biosphere likely replete with methane but low in sulfate. Methane at that time was a critical greenhouse gas capable of sustaining a habitable climate under relatively low solar luminosity, and relationships to iron cycling may have impacted if not dominated methane loss from the biosphere. Received 14 March 2013; accepted 31 December 2013 Corresponding author: N. Riedinger. Tel.: +1 951 827 3728; fax: +1 951 827 4324; e-mail: natascha. [email protected] *Present address: Institute of Geology and Mineralogy, University of Cologne, Cologne, Germany
INTRODUCTION Life in the deep marine biosphere and other extreme settings survives at the lower limits of nutrient and energy availability (Jørgensen & Boetius, 2007; and references therein). To do so, organisms may have to rely on yet unknown or underexplored metabolic pathways such as anaerobic oxidation of methane coupled to the reduction of highly reactive manganese and iron phases (e.g., ferrihydrite)—a process only recently demonstrated through laboratory experiments (Beal et al., 2009; Segarra et al., 2013). In many modern deep bio-
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sphere settings, for example, communities live under the co-occurrence of these electron acceptors and appreciable methane concentrations (e.g., M€arz et al., 2008), creating thermodynamically favorable conditions for iron and manganese coupled anaerobic oxidation of methane (AOM) (e.g., Konhauser et al., 2005; Thauer & Shima, 2008). Similar conditions likely prevailed in the Archean ocean, >2.5 billion years ago, known for its production and accumulation of iron oxides—in part through anoxygenic photoferrotrophy (Canfield et al., 2006; Konhauser et al., 2007)—in a biosphere presumably replete with methane but low in sulfate (Habicht
© 2014 John Wiley & Sons Ltd
Fe reduction in methane-rich sediments et al., 2002). Models suggest that up to 70% of organic matter mineralization during the Archean occurred via methanogenesis (Habicht et al., 2002). Iron-coupled AOM (FeAOM) might have regulated the amount of methane released to the atmosphere and thus its role as a greenhouse gas, along with other hydrocarbon gases linked to methane photochemistry (Haqq-Misra et al., 2008), in maintaining early habitability on Earth. Beyond its additional importance in sulfatepoor non-marine settings, such as lakes (Crowe et al., 2011; Sivan et al., 2011) and oil-contaminated aquifers (Amos et al., 2012), Fe-AOM might also be important in supporting a subsurface microbial biosphere in extraterrestrial environments. The essential requirement for Fe-AOM is the juxtaposition of elevated methane concentrations and abundant reactive Fe (III) in the absence of appreciable reactive organic matter, although the relative kinetic favorability of the competing pathways is not known. In the sulfate-rich modern ocean, such requirements demand special but not unusual depositional conditions that can be found in numerous marine settings (e.g., Aller et al., 1986; Kasten et al., 1998; Jørgensen et al., 2004; M€arz et al., 2008). These conditions are well expressed in the Argentine Basin off the coast of Uruguay and Argentina, in the southern Atlantic Ocean (Hensen et al., 2003; Riedinger et al., 2005). Here, we present a comprehensive inorganic geochemical data set from the natural marine setting of the Argentine Basin using sediment cores taken during R/V Meteor expedition M78/3. The non-steady state sedimentary environment along the continental margin off Argentina is characterized by mass movements and attendant turbidity currents (Henkel et al., 2011; Krastel et al., 2011a; Preu et al., 2013). Erosion and downslope transport of iron sulfide-containing sediments in the presence of oxic seawater results in the oxidation of iron monosulfide minerals and fine-grained pyrite to amorphous ferric hydroxides (Morse, 1991). These particular depositional conditions also deliver mostly reworked organic matter to deeper marine sediments in the Argentine Basin (Hensen et al., 2000; Frenz et al., 2003), resulting in dilution and subsequent burial of comparatively unreactive, remineralized indigenous organic compounds (Hedges & Keil, 1995). Riedinger et al. (2005) showed that a high mean sedimentation rate in the Argentine Basin area, including mass transport deposits (such as slides, slumps, or debris flow), leads to the rapid burial of reactive iron minerals present as both terrigenous phases and reworked and oxidized authigenic components—iron sulfides in particular. In combination with moderate levels of largely reworked total organic carbon (TOC), rapid burial limits the exposure time between reactive ferric iron phases and sulfidic pore waters. The net result of this combination is the burial of intermediate sulfur phases such as elemental sulfur, as well as the survival of abundant oxidized iron and manganese phases below the sulfidic zone within the methanic zone (Hensen et al., 2003; Riedinger et al., 2005).
© 2014 John Wiley & Sons Ltd
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MATERIALS AND METHODS Sampling and sample processing The investigated gravity cores—GeoB 13863-1 (39°18.70′S, 53°57.16′W) and GeoB 13820-1 (39°18.06′S, 53°58.03′ W)—were retrieved east of the Rio de la Plata from water depths of 3687 and 3613 m, respectively, during R/V Meteor expedition M78/3 in May–July 2009. Immediately after recovery, the cores were cut into 1-m segments on deck, and 3 mL syringe samples were taken from every segment for methane analysis. The samples were transferred into 20-mL headspace vials, which were pre-filled with 10 mL of a 5 M NaCl solution. The headspace vials were closed, shaken, inverted, and stored at 4 °C pending analysis onshore. The cores were then split, and one-half was transferred immediately into a cool room (~4 °C) where pore waters were sampled right away using rhizons (Seeberg-Elverfeldt et al., 2005; Dickens et al., 2007) with a pore size of ~0.1–0.2 lm. The first ~0.5 mL from each syringe, potentially prone to oxidation due to oxygen in the tubing of the rhizons, was discarded. For sulfate and hydrogen sulfide analysis, 5 mL subsamples of the pore water were added to a 2.5% ZnAc solution in order to fix all sulfide present as ZnS. Subsamples for cation analysis were acidified with concentrated (12 M), supra-pure HCl. All pore water samples were stored at 4 °C. The pH was determined using a punch-in electrode. Solid-phase samples for total digestions, sequential extractions, and mineralogical analyses were taken at 20- to 30-cm intervals and were sealed under a nitrogen atmosphere in aluminum bags to avoid oxidation of reduced species. The storage temperature for all sediments was 20 °C. The use of a gravity core usually results in the loss of the uppermost sediments (~5–20 cm). At the investigated sites, the concentration profiles for Mn and Fe indicate that the oxic layer, along with parts of the uppermost post-oxic layer, was not recovered. These lost layers are very shallow and so represent only minimal loss that does not impact the records of processes in the deeper sediments—the focus of this study. All sample preparations and analyses were carried out at the University of California Riverside, if not indicated otherwise. The geochemical data reported here can be accessed via the information system PANGAEA operated by the World Data Centers for Marine Environmental Sciences (http://www.pangaea.de/PangaVista). Pore water analyses Sulfate measurements for samples of core GeoB 13820-1 were performed onboard the ship using a high-performance liquid chromatography (HPLC) Sykam solvent delivery system coupled to a Waters 430 conductivity detector. Sulfate
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concentrations for site GeoB 13863 were measured by suppressed ion chromatography at a 1:100 dilution with 18 MΩ water on a Metrohm 761 compact IC at the Max Planck Institute for Marine Microbiology, Bremen, Germany (MPI-MM). We performed standard calibrations using seawater provided by the International Association for the Physical Sciences of the Oceans and in-house standards. Replicate analyses had an error of
DOI: 10.1111/gbi.12077
An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments N. RIEDINGER,1 M. J. FORMOLO,2 T. W. LYONS,1 S. HENKEL,3,* A. BECK4 AND S. KASTEN3,5 1
Department of Earth Sciences, University of California, Riverside, CA, USA Department of Geosciences, The University of Tulsa, Tulsa, OK, USA 3 Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany 4 Center for Geomicrobiology, Aarhus University, Aarhus C, Denmark 5 MARUM - Center for Marine Environmental Sciences and Department of Geosciences, University of Bremen, Bremen, Germany 2
ABSTRACT Here, we present results from sediments collected in the Argentine Basin, a non-steady state depositional marine system characterized by abundant oxidized iron within methane-rich layers due to sediment reworking followed by rapid deposition. Our comprehensive inorganic data set shows that iron reduction in these sulfate and sulfide-depleted sediments is best explained by a microbially mediated process—implicating anaerobic oxidation of methane coupled to iron reduction (Fe-AOM) as the most likely major mechanism. Although important in many modern marine environments, iron-driven AOM may not consume similar amounts of methane compared with sulfate-dependent AOM. Nevertheless, it may have broad impact on the deep biosphere and dominate both iron and methane cycling in sulfate-lean marine settings. Fe-AOM might have been particularly relevant in the Archean ocean, >2.5 billion years ago, known for its production and accumulation of iron oxides (in iron formations) in a biosphere likely replete with methane but low in sulfate. Methane at that time was a critical greenhouse gas capable of sustaining a habitable climate under relatively low solar luminosity, and relationships to iron cycling may have impacted if not dominated methane loss from the biosphere. Received 14 March 2013; accepted 31 December 2013 Corresponding author: N. Riedinger. Tel.: +1 951 827 3728; fax: +1 951 827 4324; e-mail: natascha. [email protected] *Present address: Institute of Geology and Mineralogy, University of Cologne, Cologne, Germany
INTRODUCTION Life in the deep marine biosphere and other extreme settings survives at the lower limits of nutrient and energy availability (Jørgensen & Boetius, 2007; and references therein). To do so, organisms may have to rely on yet unknown or underexplored metabolic pathways such as anaerobic oxidation of methane coupled to the reduction of highly reactive manganese and iron phases (e.g., ferrihydrite)—a process only recently demonstrated through laboratory experiments (Beal et al., 2009; Segarra et al., 2013). In many modern deep bio-
172
sphere settings, for example, communities live under the co-occurrence of these electron acceptors and appreciable methane concentrations (e.g., M€arz et al., 2008), creating thermodynamically favorable conditions for iron and manganese coupled anaerobic oxidation of methane (AOM) (e.g., Konhauser et al., 2005; Thauer & Shima, 2008). Similar conditions likely prevailed in the Archean ocean, >2.5 billion years ago, known for its production and accumulation of iron oxides—in part through anoxygenic photoferrotrophy (Canfield et al., 2006; Konhauser et al., 2007)—in a biosphere presumably replete with methane but low in sulfate (Habicht
© 2014 John Wiley & Sons Ltd
Fe reduction in methane-rich sediments et al., 2002). Models suggest that up to 70% of organic matter mineralization during the Archean occurred via methanogenesis (Habicht et al., 2002). Iron-coupled AOM (FeAOM) might have regulated the amount of methane released to the atmosphere and thus its role as a greenhouse gas, along with other hydrocarbon gases linked to methane photochemistry (Haqq-Misra et al., 2008), in maintaining early habitability on Earth. Beyond its additional importance in sulfatepoor non-marine settings, such as lakes (Crowe et al., 2011; Sivan et al., 2011) and oil-contaminated aquifers (Amos et al., 2012), Fe-AOM might also be important in supporting a subsurface microbial biosphere in extraterrestrial environments. The essential requirement for Fe-AOM is the juxtaposition of elevated methane concentrations and abundant reactive Fe (III) in the absence of appreciable reactive organic matter, although the relative kinetic favorability of the competing pathways is not known. In the sulfate-rich modern ocean, such requirements demand special but not unusual depositional conditions that can be found in numerous marine settings (e.g., Aller et al., 1986; Kasten et al., 1998; Jørgensen et al., 2004; M€arz et al., 2008). These conditions are well expressed in the Argentine Basin off the coast of Uruguay and Argentina, in the southern Atlantic Ocean (Hensen et al., 2003; Riedinger et al., 2005). Here, we present a comprehensive inorganic geochemical data set from the natural marine setting of the Argentine Basin using sediment cores taken during R/V Meteor expedition M78/3. The non-steady state sedimentary environment along the continental margin off Argentina is characterized by mass movements and attendant turbidity currents (Henkel et al., 2011; Krastel et al., 2011a; Preu et al., 2013). Erosion and downslope transport of iron sulfide-containing sediments in the presence of oxic seawater results in the oxidation of iron monosulfide minerals and fine-grained pyrite to amorphous ferric hydroxides (Morse, 1991). These particular depositional conditions also deliver mostly reworked organic matter to deeper marine sediments in the Argentine Basin (Hensen et al., 2000; Frenz et al., 2003), resulting in dilution and subsequent burial of comparatively unreactive, remineralized indigenous organic compounds (Hedges & Keil, 1995). Riedinger et al. (2005) showed that a high mean sedimentation rate in the Argentine Basin area, including mass transport deposits (such as slides, slumps, or debris flow), leads to the rapid burial of reactive iron minerals present as both terrigenous phases and reworked and oxidized authigenic components—iron sulfides in particular. In combination with moderate levels of largely reworked total organic carbon (TOC), rapid burial limits the exposure time between reactive ferric iron phases and sulfidic pore waters. The net result of this combination is the burial of intermediate sulfur phases such as elemental sulfur, as well as the survival of abundant oxidized iron and manganese phases below the sulfidic zone within the methanic zone (Hensen et al., 2003; Riedinger et al., 2005).
© 2014 John Wiley & Sons Ltd
173
MATERIALS AND METHODS Sampling and sample processing The investigated gravity cores—GeoB 13863-1 (39°18.70′S, 53°57.16′W) and GeoB 13820-1 (39°18.06′S, 53°58.03′ W)—were retrieved east of the Rio de la Plata from water depths of 3687 and 3613 m, respectively, during R/V Meteor expedition M78/3 in May–July 2009. Immediately after recovery, the cores were cut into 1-m segments on deck, and 3 mL syringe samples were taken from every segment for methane analysis. The samples were transferred into 20-mL headspace vials, which were pre-filled with 10 mL of a 5 M NaCl solution. The headspace vials were closed, shaken, inverted, and stored at 4 °C pending analysis onshore. The cores were then split, and one-half was transferred immediately into a cool room (~4 °C) where pore waters were sampled right away using rhizons (Seeberg-Elverfeldt et al., 2005; Dickens et al., 2007) with a pore size of ~0.1–0.2 lm. The first ~0.5 mL from each syringe, potentially prone to oxidation due to oxygen in the tubing of the rhizons, was discarded. For sulfate and hydrogen sulfide analysis, 5 mL subsamples of the pore water were added to a 2.5% ZnAc solution in order to fix all sulfide present as ZnS. Subsamples for cation analysis were acidified with concentrated (12 M), supra-pure HCl. All pore water samples were stored at 4 °C. The pH was determined using a punch-in electrode. Solid-phase samples for total digestions, sequential extractions, and mineralogical analyses were taken at 20- to 30-cm intervals and were sealed under a nitrogen atmosphere in aluminum bags to avoid oxidation of reduced species. The storage temperature for all sediments was 20 °C. The use of a gravity core usually results in the loss of the uppermost sediments (~5–20 cm). At the investigated sites, the concentration profiles for Mn and Fe indicate that the oxic layer, along with parts of the uppermost post-oxic layer, was not recovered. These lost layers are very shallow and so represent only minimal loss that does not impact the records of processes in the deeper sediments—the focus of this study. All sample preparations and analyses were carried out at the University of California Riverside, if not indicated otherwise. The geochemical data reported here can be accessed via the information system PANGAEA operated by the World Data Centers for Marine Environmental Sciences (http://www.pangaea.de/PangaVista). Pore water analyses Sulfate measurements for samples of core GeoB 13820-1 were performed onboard the ship using a high-performance liquid chromatography (HPLC) Sykam solvent delivery system coupled to a Waters 430 conductivity detector. Sulfate
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concentrations for site GeoB 13863 were measured by suppressed ion chromatography at a 1:100 dilution with 18 MΩ water on a Metrohm 761 compact IC at the Max Planck Institute for Marine Microbiology, Bremen, Germany (MPI-MM). We performed standard calibrations using seawater provided by the International Association for the Physical Sciences of the Oceans and in-house standards. Replicate analyses had an error of
