Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps

Sivan, Orit; Antler, Gilad; Turchyn, Alexandra V.; Marlow, Jeffrey J.; Orphan, Victoria J.

doi:10.1073/pnas.1412269111

Title: Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps

Abstract

Seep sediments are dominated by intensive microbial sulfate reduction coupled to the anaerobic oxidation of methane (AOM). Through geochemical measurements of incubation experiments with methane seep sediments collected from Hydrate Ridge, we provide insight into the role of iron oxides in sulfate-driven AOM. Seep sediments incubated with ¹³C-labeled methane showed co-occurring sulfate reduction, AOM, and methanogenesis. The isotope fractionation factors for sulfur and oxygen isotopes in sulfate were about 40‰ and 22‰, respectively, reinforcing the difference between microbial sulfate reduction in methane seeps versus other sedimentary environments (for example, sulfur isotope fractionation above 60‰ in sulfate reduction coupled to organic carbon oxidation or in diffusive sedimentary sulfate–methane transition zone). The addition of hematite to these microcosm experiments resulted in significant microbial iron reduction as well as enhancing sulfate-driven AOM. The magnitude of the isotope fractionation of sulfur and oxygen isotopes in sulfate from these incubations was lowered by about 50%, indicating the involvement of iron oxides during sulfate reduction in methane seeps. The similar relative change between the oxygen versus sulfur isotopes of sulfate in all experiments (with and without hematite addition) suggests that oxidized forms of iron, naturally present in the sediment incubations, were involved in sulfate reduction, withmore »« less

Authors:

Sivan, Orit ^[1]; Antler, Gilad ^[2]; Turchyn, Alexandra V. ^[2]; Marlow, Jeffrey J. ^[3]; Orphan, Victoria J. ^[3]

Ben Gurion Univ. of the Negev, Beer-Sheva (Israel)
Univ. of Cambridge, Cambridge (United Kingdom)
California Inst. of Technology (CalTech), Pasadena, CA (United States)

Publication Date:: Mon Sep 22 00:00:00 EDT 2014

Research Org.:: California Institute of Technology (CalTech), Pasadena, CA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1455038

Grant/Contract Number:: SC0004949

Resource Type:: Accepted Manuscript

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Volume: 111; Journal Issue: 40; Journal ID: ISSN 0027-8424

Publisher:: National Academy of Sciences

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 58 GEOSCIENCES; redox; anaerobic respiration; deep-sea; methanotrophy; ANME archaea

Citation Formats


                    Sivan, Orit, Antler, Gilad, Turchyn, Alexandra V., Marlow, Jeffrey J., and Orphan, Victoria J. Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps.  United States: N. p., 2014. 
Web.  doi:10.1073/pnas.1412269111.

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                    Sivan, Orit, Antler, Gilad, Turchyn, Alexandra V., Marlow, Jeffrey J., & Orphan, Victoria J. Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps.  United States.  https://doi.org/10.1073/pnas.1412269111

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                    Sivan, Orit, Antler, Gilad, Turchyn, Alexandra V., Marlow, Jeffrey J., and Orphan, Victoria J. Mon .  
"Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps".  United States.  https://doi.org/10.1073/pnas.1412269111.  https://www.osti.gov/servlets/purl/1455038.

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@article{osti_1455038,

  title        = {Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps},

  author       = {Sivan, Orit and Antler, Gilad and Turchyn, Alexandra V. and Marlow, Jeffrey J. and Orphan, Victoria J.},

  abstractNote = {Seep sediments are dominated by intensive microbial sulfate reduction coupled to the anaerobic oxidation of methane (AOM). Through geochemical measurements of incubation experiments with methane seep sediments collected from Hydrate Ridge, we provide insight into the role of iron oxides in sulfate-driven AOM. Seep sediments incubated with 13C-labeled methane showed co-occurring sulfate reduction, AOM, and methanogenesis. The isotope fractionation factors for sulfur and oxygen isotopes in sulfate were about 40‰ and 22‰, respectively, reinforcing the difference between microbial sulfate reduction in methane seeps versus other sedimentary environments (for example, sulfur isotope fractionation above 60‰ in sulfate reduction coupled to organic carbon oxidation or in diffusive sedimentary sulfate–methane transition zone). The addition of hematite to these microcosm experiments resulted in significant microbial iron reduction as well as enhancing sulfate-driven AOM. The magnitude of the isotope fractionation of sulfur and oxygen isotopes in sulfate from these incubations was lowered by about 50%, indicating the involvement of iron oxides during sulfate reduction in methane seeps. The similar relative change between the oxygen versus sulfur isotopes of sulfate in all experiments (with and without hematite addition) suggests that oxidized forms of iron, naturally present in the sediment incubations, were involved in sulfate reduction, with hematite addition increasing the sulfate recycling or the activity of sulfur-cycling microorganisms by about 40%. Furthermore, these results highlight a role for natural iron oxides during bacterial sulfate reduction in methane seeps not only as nutrient but also as stimulator of sulfur recycling.},

  doi          = {10.1073/pnas.1412269111},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 40,

  volume       = 111,

  place        = {United States},

  year         = {Mon Sep 22 00:00:00 EDT 2014},

  month        = {Mon Sep 22 00:00:00 EDT 2014}

}

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Narrowe, Adrienne B.; Angle, Jordan C.; Daly, Rebecca A.
Environmental Microbiology, Vol. 19, Issue 6
DOI: 10.1111/1462-2920.13703

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posted_content, March 2016

Egger, Matthias; Kraal, Peter; Jilbert, Tom
Biogeosciences Discussions
DOI: 10.5194/bg-2016-64

Extreme 13C-depletions and organic sulfur content argue for S-fueled anaerobic methane oxidation in 2.72 Ga old stromatolites
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Lepot, Kevin; Williford, Kenneth H.; Philippot, Pascal
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DOI: 10.1016/j.gca.2018.10.014

Metal-dependent anaerobic methane oxidation in marine sediment: Insights from marine settings and other systems
journal, June 2019

Liang, Lewen; Wang, Yinzhao; Sivan, Orit
Science China Life Sciences, Vol. 62, Issue 10
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Manganese/iron‐supported sulfate‐dependent anaerobic oxidation of methane by archaea in lake sediments
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Su, Guangyi; Zopfi, Jakob; Yao, Haoyi
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Marlow, Jeffrey J.; Steele, Joshua A.; Ziebis, Wiebke
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Jeffrey, Luke C.; Maher, Damien T.; Johnston, Scott G.
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DOI: 10.5194/bg-16-1799-2019

Formation of large carbonate concretions in black cherts in the Gufeng Formation (Guadalupian) at Enshi, South China
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Wei, Hengye; Tang, Zhanwen; Qiu, Zhen
Geobiology, Vol. 18, Issue 1
DOI: 10.1111/gbi.12362

Rapid Sediment Accumulation Results in High Methane Effluxes from Coastal Sediments
journal, August 2016

Egger, Matthias; Lenstra, Wytze; Jong, Dirk
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DOI: 10.1371/journal.pone.0161609

Evidence for microbial iron reduction in the methanic sediments of the oligotrophic southeastern Mediterranean continental shelf
journal, January 2019

Vigderovich, Hanni; Liang, Lewen; Herut, Barak
Biogeosciences, Vol. 16, Issue 16
DOI: 10.5194/bg-16-3165-2019

Anaerobic oxidation of methane alters sediment records of sulfur, iron and phosphorus in the Black Sea
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Biogeosciences Discussions
DOI: 10.5194/bg-2016-64

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Rhizosphere to the atmosphere: contrasting methane pathways, fluxes and geochemical drivers across the terrestrial-aquatic wetland boundary
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The Apparent Involvement of ANMEs in Mineral Dependent Methane Oxidation, as an Analog for Possible Martian Methanotrophy

Journal Article House, Christopher H. ; Beal, Emily J. ; Orphan, Victoria J. - Life

On Earth, marine anaerobic methane oxidation (AOM) can be driven by the microbial reduction of sulfate, iron, and manganese. Here, we have further characterized marine sediment incubations to determine if the mineral dependent methane oxidation involves similar microorganisms to those found for sulfate-dependent methane oxidation. Through FISH and FISH-SIMS analyses using ¹³C and ¹⁵N labeled substrates, we find that the most active cells during manganese dependent AOM are primarily mixed and mixed-cluster aggregates of archaea and bacteria. Overall, our control experiment using sulfate showed two active bacterial clusters, two active shell aggregates, one active mixed aggregate, and an active archaealmore »« less
https://doi.org/10.3390/life1010019

Full Text Available
Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments

Journal Article Vigneron, Adrien ; Alsop, Eric B. ; Cruaud, Perrine ; ... - mSystems

Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investigate microbial function and activities in these ecosystems, metabolic potential (metagenomic) and gene expression (metatranscriptomic) analyses of two cold seep areas of the Gulf of Mexico were carried out. Seeps emitting biogenic methane harbored microbial communities dominated by archaeal anaerobic methane oxidizers of phylogenetic group 1 (ANME-1), whereas seeps producing fluids containing a complex mixture of thermogenic hydrocarbons were dominated by ANME-2more »« less
Cited by 22
https://doi.org/10.1128/mSystems.00091-18

Full Text Available
Microbial sulfate reduction rates and sulfur and oxygen isotope fractionations at oil and gas seeps in deepwater Gulf of Mexico

Journal Article Aharon, P ; Fu, B - Geochimica et Cosmochimica Acta

sulfate reduction and anaerobic methane oxidation are the dominant microbial processes occurring in hydrate-bearing sediments at bathyal depths in the Gulf of Mexico where crude oil and methane are advecting through fault conduits to the seafloor. The oil and gas seeps are typically overlain by chemosynthetic communities consisting of thiotrophic bacterial mats (Beggiatoa spp.) and methanotrophic mussels (Bathymodiolus spp.), respectively. Cores were recovered with a manned submersible from fine-grained sediments containing dispersed gas hydrates at the threshold of stability. Estimated sulfate reduction rates are variable but generally are substantially higher in crude oil seeps (up to 50 times) and methanemore »« less
https://doi.org/10.1016/S0016-7037(99)00292-6
Isolating Detrital and Diagenetic Signals in Magnetic Susceptibility Records From Methane‐Bearing Marine Sediments

Journal Article Johnson, Joel E. ; Phillips, Stephen C. ; Clyde, William C. ; ... - Geochemistry, Geophysics, Geosystems

Abstract Volume‐dependent magnetic susceptibility (κ) is commonly used for paleoenvironmental reconstructions in both terrestrial and marine sedimentary environments where it reflects a mixed signal between primary deposition and secondary diagenesis. In the marine environment, κ is strongly influenced by the abundance of ferrimagnetic minerals regulated by sediment transport processes. Post‐depositional alteration by H ₂ S, however, can dissolve titanomagnetite, releasing reactive Fe that promotes pyritization and subsequently decreases κ. Here, we provide a new approach for isolating the detrital signal in κ and identifying intervals of diagenetic alteration of κ driven by organoclastic sulfate reduction (OSR) and the anaerobic oxidationmore »« less
https://doi.org/10.1029/2021GC009867
Characterization of microbial associations with methanotrophic archaea and sulfate-reducing bacteria through statistical comparison of nested Magneto-FISH enrichments

Journal Article Trembath-Reichert, Elizabeth ; Case, David H. ; Orphan, Victoria J. - PeerJ

Methane seep systems along continental margins host diverse and dynamic microbial assemblages, sustained in large part through the microbially mediated process of sulfate-coupled Anaerobic Oxidation of Methane (AOM). This methanotrophic metabolism has been linked to consortia of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). These two groups are the focus of numerous studies; however, less is known about the wide diversity of other seep associated microorganisms. We selected a hierarchical set of FISH probes targeting a range ofDeltaproteobacteriadiversity. Using the Magneto-FISH enrichment technique, we then magnetically captured CARD-FISH hybridized cells and their physically associated microorganisms from a methane seepmore »« less
Cited by 27
https://doi.org/10.7717/peerj.1913

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Title: Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps

Abstract

Citation Formats

Stable isotope tracing of anaerobic methane oxidation in the gassy sediments of Eckernfoerde Bay, German Baltic Sea journal, November 1999

Ferrozine---a new spectrophotometric reagent for iron journal, June 1970

Kinetic oxygen isotope effects during dissimilatory sulfate reduction: A combined theoretical and experimental approach journal, April 2010

Effects of Iron and Nitrogen Limitation on Sulfur Isotope Fractionation during Microbial Sulfate Reduction journal, September 2012

A microbial consortium couples anaerobic methane oxidation to denitrification journal, April 2006

Enrichment and Molecular Detection of Denitrifying Methanotrophic Bacteria of the NC10 Phylum journal, March 2009

Stable isotope fractionation during bacterial sulfate reduction is controlled by reoxidation of intermediates journal, September 2007

Manganese- and Iron-Dependent Marine Methane Oxidation journal, July 2009

Fates of methane from different lake habitats: Connecting whole-lake budgets and CH 4 emissions : FATES OF LAKE METHANE journal, May 2008

Hypersulfidic deep biosphere indicates extreme sulfur isotope fractionation during single-step microbial sulfate reduction journal, January 2001

Anaerobic oxidation of methane in an iron-rich Danish freshwater lake sediment journal, February 2013

Anaerobic oxidation of methane by sulfate in hypersaline groundwater of the Dead Sea aquifer journal, July 2014

Sulfate reduction and related stable isotope (34S, 18O) variations in interstitial waters from the Eastern Mediterranean book, September 1998

An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments journal, January 2014

Rates of methanogenesis and methanotrophy in deep-sea sediments journal, June 2007

Ferrihydrite-Dependent Growth of Sulfurospirillum deleyianum through Electron Transfer via Sulfur Cycling journal, October 2004

A cryptic sulfur cycle driven by iron in the methane zone of marine sediment (Aarhus Bay, Denmark) journal, June 2011

Effect of electron donors on the fractionation of sulfur isotopes by a marine Desulfovibrio sp. journal, August 2011

Microbially mediated re-oxidation of sulfide during dissimilatory sulfate reduction by Desulfobacter latus journal, June 2011

Coupled sulfur and oxygen isotope insight into bacterial sulfate reduction in the natural environment journal, October 2013

Sulfur and oxygen isotope tracing of sulfate driven anaerobic methane oxidation in estuarine sediments journal, April 2014

Anaerobic Methane Oxidation: Occurrence and Ecology journal, January 1980

Biogenic methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation—Isotope evidence journal, May 1986

A model for oxygen and sulfur isotope fractionation in sulfate during bacterial sulfate reduction processes journal, October 2005

Nitrate-dependent anaerobic methane oxidation in a freshwater sediment journal, May 2014

Large Sulfur Isotope Fractionation Does Not Require Disproportionation journal, June 2011

The reactivity of iron oxides in sediments: A kinetic approach journal, November 1993

Carbon, sulfur, and oxygen isotope geochemistry of interstitial waters from the western Mediterranean book, February 1999

Nitrite-driven anaerobic methane oxidation by oxygenic bacteria journal, March 2010

Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane journal, September 1999

Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor journal, September 2003

Zero-valent sulphur is a key intermediate in marine methane oxidation journal, November 2012

Temperature and its control of isotope fractionation by a sulfate-reducing bacterium journal, February 2006

Methane-Consuming Archaea Revealed by Directly Coupled Isotopic and Phylogenetic Analysis journal, July 2001

Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis journal, July 1979

Carbon and sulfur back flux during anaerobic microbial oxidation of methane and coupled sulfate reduction journal, December 2011

Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities journal, January 2005

Methane and microbes journal, April 2006

Microbial sulfate reduction rates and sulfur and oxygen isotope fractionations at oil and gas seeps in deepwater Gulf of Mexico journal, January 2000

Determination and application of the equilibrium oxygen isotope effect between water and sulfite journal, January 2014

Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen-sulfate reducer consortium journal, December 1994

Microbiological Fractionation of Sulphur Isotopes journal, February 1964

Patterns of 15 N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS journal, July 2009

Carbon isotope equilibration during sulphate-limited anaerobic oxidation of methane journal, January 2014

Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review journal, January 2002

Sulfate Reduction in Marine Sediments book, January 2000

Bacterial enzymes for dissimilatory sulfate reduction in a marine microbial mat (Black Sea) mediating anaerobic oxidation of methane: Sulfate-reducing enzymes from a Black Sea microbial mat journal, March 2011

The role of highly sratified nutrient-rich small estuaries as a source of dissolved inorganic nitrogen to coastal seawater, the Qishon (SE Mediterranean) case journal, June 2013

Deep Sulfate Reduction Completely Mediated by Anaerobic Methane Oxidation in Sediments of the Upwelling Area off Namibia journal, February 1998

A revised isotope fractionation model for dissimilatory sulfate reduction in sulfate reducing bacteria journal, October 2005

Carbon and hydrogen isotope fractionation resulting from anaerobic methane oxidation journal, September 1988

Geochemical evidence for iron-mediated anaerobic oxidation of methane journal, July 2011

Sulfur isotope fractionation during bacterial sulfate reduction in organic-rich sediments journal, December 1997

Sulfur and oxygen isotopes of coeval sulfate–sulfide in pore fluids of cold seep sediments with sharp redox gradients journal, April 2003

The reversibility of dissimilatory sulphate reduction and the cell-internal multi-step reduction of sulphite to sulphide: insights from the oxygen isotope composition of sulphate journal, March 2012

Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage journal, July 2013

Multiple sulphur isotopic interpretations of biosynthetic pathways: implications for biological signatures in the sulphur isotope record journal, July 2003

Oxygen isotope biogeochemistry of pore water sulfate in the deep biosphere: Dominance of isotope exchange reactions with ambient water during microbial sulfate reduction (ODP Site 1130) journal, September 2007

Fractionation of sulfur isotopes by continuous cultures of Desulfovibrio desulfuricans journal, October 1975

Benthic sulfate reduction along the Chesapeake Bay central channel. II. Temporal controls journal, January 2003

A marine microbial consortium apparently mediating anaerobic oxidation of methane journal, October 2000

A steady-state model for sulphur isotope fractionation in bacterial reduction processes journal, May 1973

Quantifying rates of methanogenesis and methanotrophy in Lake Kinneret sediments (Israel) using pore-water profiles journal, July 2011

Ferrihydrite reduction by Geobacter species is stimulated by secondary bacteria journal, August 2004

The biogeochemistry of sorbed methane in marine sediments journal, November 2010

Sulfur and oxygen isotope fractionation during sulfate reduction coupled to anaerobic oxidation of methane is dependent on methane concentration journal, August 2014

Extensive carbon isotopic heterogeneity among methane seep microbiota journal, September 2009

Interstitial water chemistry of anoxic Long Island Sound sediments. 1. Dissolved gases1: Dissolved gases in sediments journal, January 1977

Oxygen isotopic composition of sulfate in deep sea pore fluid: evidence for rapid sulfur cycling journal, September 2006

12. Biogeochemistry of Sulfur Isotopes book, January 2001

Enhancement of Biological Reduction of Hematite by Electron Shuttling and Fe(II) Complexation journal, May 2002

Marine pore-water sulfate profiles indicate in situ methane flux from underlying gas hydrate journal, January 1996

Biogeochemistry of Sulfur Isotopes journal, January 2001

Co-existence of Methanogenesis and Sulfate Reduction with Common Substrates in Sulfate-Rich Estuarine Sediments journal, May 2017

Iron-dependent anaerobic oxidation of methane in coastal surface sediments: Potential controls and impact: Iron-dependent oxidation of methane journal, April 2016

Rates and pathways of CH 4 oxidation in ferruginous Lake Matano, Indonesia journal, December 2018

A Review of Landfill Microbiology and Ecology: A Call for Modernization With ‘Next Generation’ Technology journal, June 2020

Stable isotope tracing of anaerobic methane oxidation in the gassy sediments of Eckernfoerde Bay, German Baltic Sea
journal, November 1999

Ferrozine---a new spectrophotometric reagent for iron
journal, June 1970

Kinetic oxygen isotope effects during dissimilatory sulfate reduction: A combined theoretical and experimental approach
journal, April 2010

Effects of Iron and Nitrogen Limitation on Sulfur Isotope Fractionation during Microbial Sulfate Reduction
journal, September 2012

A microbial consortium couples anaerobic methane oxidation to denitrification
journal, April 2006

Enrichment and Molecular Detection of Denitrifying Methanotrophic Bacteria of the NC10 Phylum
journal, March 2009

Stable isotope fractionation during bacterial sulfate reduction is controlled by reoxidation of intermediates
journal, September 2007

Manganese- and Iron-Dependent Marine Methane Oxidation
journal, July 2009

Fates of methane from different lake habitats: Connecting whole-lake budgets and CH ₄ emissions : FATES OF LAKE METHANE
journal, May 2008

Hypersulfidic deep biosphere indicates extreme sulfur isotope fractionation during single-step microbial sulfate reduction
journal, January 2001

Anaerobic oxidation of methane in an iron-rich Danish freshwater lake sediment
journal, February 2013

Anaerobic oxidation of methane by sulfate in hypersaline groundwater of the Dead Sea aquifer
journal, July 2014

Sulfate reduction and related stable isotope (³⁴S, ¹⁸O) variations in interstitial waters from the Eastern Mediterranean
book, September 1998

An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments
journal, January 2014

Rates of methanogenesis and methanotrophy in deep-sea sediments
journal, June 2007

Ferrihydrite-Dependent Growth of Sulfurospirillum deleyianum through Electron Transfer via Sulfur Cycling
journal, October 2004

A cryptic sulfur cycle driven by iron in the methane zone of marine sediment (Aarhus Bay, Denmark)
journal, June 2011

Effect of electron donors on the fractionation of sulfur isotopes by a marine Desulfovibrio sp.
journal, August 2011

Microbially mediated re-oxidation of sulfide during dissimilatory sulfate reduction by Desulfobacter latus
journal, June 2011

Coupled sulfur and oxygen isotope insight into bacterial sulfate reduction in the natural environment
journal, October 2013

Sulfur and oxygen isotope tracing of sulfate driven anaerobic methane oxidation in estuarine sediments
journal, April 2014

Anaerobic Methane Oxidation: Occurrence and Ecology
journal, January 1980

Biogenic methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation—Isotope evidence
journal, May 1986

A model for oxygen and sulfur isotope fractionation in sulfate during bacterial sulfate reduction processes
journal, October 2005

Nitrate-dependent anaerobic methane oxidation in a freshwater sediment
journal, May 2014

Large Sulfur Isotope Fractionation Does Not Require Disproportionation
journal, June 2011

The reactivity of iron oxides in sediments: A kinetic approach
journal, November 1993

Carbon, sulfur, and oxygen isotope geochemistry of interstitial waters from the western Mediterranean
book, February 1999

Nitrite-driven anaerobic methane oxidation by oxygenic bacteria
journal, March 2010

Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane
journal, September 1999

Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor
journal, September 2003

Zero-valent sulphur is a key intermediate in marine methane oxidation
journal, November 2012

Temperature and its control of isotope fractionation by a sulfate-reducing bacterium
journal, February 2006

Methane-Consuming Archaea Revealed by Directly Coupled Isotopic and Phylogenetic Analysis
journal, July 2001

Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis
journal, July 1979

Carbon and sulfur back flux during anaerobic microbial oxidation of methane and coupled sulfate reduction
journal, December 2011

Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities
journal, January 2005

Methane and microbes
journal, April 2006

Microbial sulfate reduction rates and sulfur and oxygen isotope fractionations at oil and gas seeps in deepwater Gulf of Mexico
journal, January 2000

Determination and application of the equilibrium oxygen isotope effect between water and sulfite
journal, January 2014

Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen-sulfate reducer consortium
journal, December 1994

Microbiological Fractionation of Sulphur Isotopes
journal, February 1964

Patterns of ¹⁵ N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS
journal, July 2009

Carbon isotope equilibration during sulphate-limited anaerobic oxidation of methane
journal, January 2014

Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review
journal, January 2002

Sulfate Reduction in Marine Sediments
book, January 2000

Bacterial enzymes for dissimilatory sulfate reduction in a marine microbial mat (Black Sea) mediating anaerobic oxidation of methane: Sulfate-reducing enzymes from a Black Sea microbial mat
journal, March 2011

The role of highly sratified nutrient-rich small estuaries as a source of dissolved inorganic nitrogen to coastal seawater, the Qishon (SE Mediterranean) case
journal, June 2013

Deep Sulfate Reduction Completely Mediated by Anaerobic Methane Oxidation in Sediments of the Upwelling Area off Namibia
journal, February 1998

A revised isotope fractionation model for dissimilatory sulfate reduction in sulfate reducing bacteria
journal, October 2005

Carbon and hydrogen isotope fractionation resulting from anaerobic methane oxidation
journal, September 1988

Geochemical evidence for iron-mediated anaerobic oxidation of methane
journal, July 2011

Sulfur isotope fractionation during bacterial sulfate reduction in organic-rich sediments
journal, December 1997

Sulfur and oxygen isotopes of coeval sulfate–sulfide in pore fluids of cold seep sediments with sharp redox gradients
journal, April 2003

The reversibility of dissimilatory sulphate reduction and the cell-internal multi-step reduction of sulphite to sulphide: insights from the oxygen isotope composition of sulphate
journal, March 2012

Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage
journal, July 2013

Multiple sulphur isotopic interpretations of biosynthetic pathways: implications for biological signatures in the sulphur isotope record
journal, July 2003

Oxygen isotope biogeochemistry of pore water sulfate in the deep biosphere: Dominance of isotope exchange reactions with ambient water during microbial sulfate reduction (ODP Site 1130)
journal, September 2007

Fractionation of sulfur isotopes by continuous cultures of Desulfovibrio desulfuricans
journal, October 1975

Benthic sulfate reduction along the Chesapeake Bay central channel. II. Temporal controls
journal, January 2003

A marine microbial consortium apparently mediating anaerobic oxidation of methane
journal, October 2000

A steady-state model for sulphur isotope fractionation in bacterial reduction processes
journal, May 1973

Quantifying rates of methanogenesis and methanotrophy in Lake Kinneret sediments (Israel) using pore-water profiles
journal, July 2011

Ferrihydrite reduction by Geobacter species is stimulated by secondary bacteria
journal, August 2004

The biogeochemistry of sorbed methane in marine sediments
journal, November 2010

Sulfur and oxygen isotope fractionation during sulfate reduction coupled to anaerobic oxidation of methane is dependent on methane concentration
journal, August 2014

Extensive carbon isotopic heterogeneity among methane seep microbiota
journal, September 2009

Interstitial water chemistry of anoxic Long Island Sound sediments. 1. Dissolved gases1: Dissolved gases in sediments
journal, January 1977

Oxygen isotopic composition of sulfate in deep sea pore fluid: evidence for rapid sulfur cycling
journal, September 2006

12. Biogeochemistry of Sulfur Isotopes
book, January 2001

Enhancement of Biological Reduction of Hematite by Electron Shuttling and Fe(II) Complexation
journal, May 2002

Marine pore-water sulfate profiles indicate in situ methane flux from underlying gas hydrate
journal, January 1996

Biogeochemistry of Sulfur Isotopes
journal, January 2001

Co-existence of Methanogenesis and Sulfate Reduction with Common Substrates in Sulfate-Rich Estuarine Sediments
journal, May 2017

Iron-dependent anaerobic oxidation of methane in coastal surface sediments: Potential controls and impact: Iron-dependent oxidation of methane
journal, April 2016

Rates and pathways of CH ₄ oxidation in ferruginous Lake Matano, Indonesia
journal, December 2018

A Review of Landfill Microbiology and Ecology: A Call for Modernization With ‘Next Generation’ Technology
journal, June 2020

Co-existence of Methanogenesis and Sulfate Reduction with Common Substrates in Sulfate-Rich Estuarine Sediments
journal, May 2017

Global diffusive fluxes of methane in marine sediments
journal, May 2018

Rhizosphere to the atmosphere: contrasting methane pathways, fluxes and geochemical drivers across the terrestrial-aquatic wetland boundary
posted_content, January 2019