Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin

Philip Eickenbusch* (Corresponding Author), Ken Takai, Olivier Sissman, Shino Suzuki, Catriona Menzies, Sanae Sakai, Pierre Sansjofre, Eiji Tasumi, Stefano M. Bernasconi, Clemens Glombitza, Bo Barker Jørgensen, Yuki Morono, Mark Alexander Lever (Corresponding Author)

*Corresponding author for this work

Research output: Contribution to journalArticle

Abstract

Serpentinitic systems are potential habitats for microbial life due to frequently high concentrations of microbial energy substrates, such as hydrogen (H2), methane (CH4), and short-chain organic acids (SCOAs). Yet, many serpentinitic systems are also physiologically challenging environments due to highly alkaline conditions (pH > 10) and elevated temperatures (>80.C). To elucidate the possibility of microbial life in deep serpentinitic crustal environments, International Ocean Discovery Program (IODP) Expedition 366 drilled into the Yinazao, Fantangisna, and Asut Tesoru serpentinite mud volcanoes on the Mariana Forearc. These mud volcanoes differ in temperature (80, 150, 250.C, respectively) of the underlying subducting slab, and in the porewater pH (11.0, 11.2, 12.5, respectively) of the serpentinite mud. Increases in formate and acetate concentrations across the three mud volcanoes, which are positively correlated with temperature in the subducting slab and coincide with strong increases in H2 concentrations, indicate a serpentinization-related origin. Thermodynamic calculations suggest that formate is produced by equilibrium reactions with dissolved inorganic carbon (DIC) + H2, and that equilibration continues during fluid ascent at temperatures below 80.C. By contrast, the mechanism(s) of acetate production are not clear. Besides formate, acetate, and H2 data, we present concentrations of other SCOAs, methane, carbon monoxide, and sulfate, d13C-data on bulk carbon pools, and microbial cell counts. Even though calculations indicate a wide range of microbial catabolic reactions to be thermodynamically favorable, concentration profiles of potential energy substrates, and very low cell numbers suggest that microbial life is scarce or absent. We discuss the potential roles of temperature, pH, pressure, and dispersal in limiting the occurrence of microbial life in deep serpentinitic environments.

Original languageEnglish
Article number1729
Number of pages21
JournalFrontiers in Microbiology
Volume10
DOIs
Publication statusPublished - 26 Jul 2019

Fingerprint

formic acid
Temperature
Acids
Acetates
Methane
Carbon
Cell Count
Expeditions
Carbon Monoxide
Thermodynamics
Oceans and Seas
Sulfates
Ecosystem
Hydrogen
Pressure

Keywords

  • Abiotic synthesis
  • Acetate
  • Deep biosphere
  • Formate
  • International ocean discovery program
  • Limits of life
  • Methane
  • Serpentinization
  • deep biosphere
  • HYDROGEN GENERATION
  • FORE-ARC
  • acetate
  • formate
  • MICROBIAL COMMUNITIES
  • ACTIVITY-COEFFICIENTS
  • ANAEROBIC-BACTERIA
  • REDUCING BACTERIA
  • limits of life
  • International Ocean Discovery Program
  • VOLATILE FATTY-ACIDS
  • DEEP SUBSEAFLOOR SEDIMENTS
  • HYDROTHERMAL REACTIVITY
  • serpentinization
  • abiotic synthesis
  • methane
  • THERMOCHEMICAL SULFATE REDUCTION

ASJC Scopus subject areas

  • Microbiology (medical)
  • Microbiology

Cite this

Eickenbusch, P., Takai, K., Sissman, O., Suzuki, S., Menzies, C., Sakai, S., ... Lever, M. A. (2019). Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin. Frontiers in Microbiology, 10, [1729]. https://doi.org/10.3389/fmicb.2019.01729

Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin. / Eickenbusch, Philip (Corresponding Author); Takai, Ken; Sissman, Olivier; Suzuki, Shino; Menzies, Catriona; Sakai, Sanae; Sansjofre, Pierre; Tasumi, Eiji; Bernasconi, Stefano M.; Glombitza, Clemens; Jørgensen, Bo Barker; Morono, Yuki; Lever, Mark Alexander (Corresponding Author).

In: Frontiers in Microbiology, Vol. 10, 1729, 26.07.2019.

Research output: Contribution to journalArticle

Eickenbusch, P, Takai, K, Sissman, O, Suzuki, S, Menzies, C, Sakai, S, Sansjofre, P, Tasumi, E, Bernasconi, SM, Glombitza, C, Jørgensen, BB, Morono, Y & Lever, MA 2019, 'Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin', Frontiers in Microbiology, vol. 10, 1729. https://doi.org/10.3389/fmicb.2019.01729
Eickenbusch, Philip ; Takai, Ken ; Sissman, Olivier ; Suzuki, Shino ; Menzies, Catriona ; Sakai, Sanae ; Sansjofre, Pierre ; Tasumi, Eiji ; Bernasconi, Stefano M. ; Glombitza, Clemens ; Jørgensen, Bo Barker ; Morono, Yuki ; Lever, Mark Alexander. / Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin. In: Frontiers in Microbiology. 2019 ; Vol. 10.
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abstract = "Serpentinitic systems are potential habitats for microbial life due to frequently high concentrations of microbial energy substrates, such as hydrogen (H2), methane (CH4), and short-chain organic acids (SCOAs). Yet, many serpentinitic systems are also physiologically challenging environments due to highly alkaline conditions (pH > 10) and elevated temperatures (>80.C). To elucidate the possibility of microbial life in deep serpentinitic crustal environments, International Ocean Discovery Program (IODP) Expedition 366 drilled into the Yinazao, Fantangisna, and Asut Tesoru serpentinite mud volcanoes on the Mariana Forearc. These mud volcanoes differ in temperature (80, 150, 250.C, respectively) of the underlying subducting slab, and in the porewater pH (11.0, 11.2, 12.5, respectively) of the serpentinite mud. Increases in formate and acetate concentrations across the three mud volcanoes, which are positively correlated with temperature in the subducting slab and coincide with strong increases in H2 concentrations, indicate a serpentinization-related origin. Thermodynamic calculations suggest that formate is produced by equilibrium reactions with dissolved inorganic carbon (DIC) + H2, and that equilibration continues during fluid ascent at temperatures below 80.C. By contrast, the mechanism(s) of acetate production are not clear. Besides formate, acetate, and H2 data, we present concentrations of other SCOAs, methane, carbon monoxide, and sulfate, d13C-data on bulk carbon pools, and microbial cell counts. Even though calculations indicate a wide range of microbial catabolic reactions to be thermodynamically favorable, concentration profiles of potential energy substrates, and very low cell numbers suggest that microbial life is scarce or absent. We discuss the potential roles of temperature, pH, pressure, and dispersal in limiting the occurrence of microbial life in deep serpentinitic environments.",
keywords = "Abiotic synthesis, Acetate, Deep biosphere, Formate, International ocean discovery program, Limits of life, Methane, Serpentinization, deep biosphere, HYDROGEN GENERATION, FORE-ARC, acetate, formate, MICROBIAL COMMUNITIES, ACTIVITY-COEFFICIENTS, ANAEROBIC-BACTERIA, REDUCING BACTERIA, limits of life, International Ocean Discovery Program, VOLATILE FATTY-ACIDS, DEEP SUBSEAFLOOR SEDIMENTS, HYDROTHERMAL REACTIVITY, serpentinization, abiotic synthesis, methane, THERMOCHEMICAL SULFATE REDUCTION",
author = "Philip Eickenbusch and Ken Takai and Olivier Sissman and Shino Suzuki and Catriona Menzies and Sanae Sakai and Pierre Sansjofre and Eiji Tasumi and Bernasconi, {Stefano M.} and Clemens Glombitza and J{\o}rgensen, {Bo Barker} and Yuki Morono and Lever, {Mark Alexander}",
note = "Funding This research used samples and/or data provided by the International Ocean Discovery Program (IODP). Additional support for the participation in IODP Expedition came from SwissDrilling (www.swissdrilling.ch), which is funded by the Swiss National Science Foundation (SNSF; www.snf.ch) project No. 182091 and by the Deep Carbon Observatory (www.deepcarbon.net). Funding for this research was provided by ETH Zurich. CG and BJ were supported by the Danish National Research Foundation [DNRF104], the European Research Council [ERC Advanced Grant #294200], and the Danish Council for Independent Research [DFF−7014-00196]. CM was supported by a NERC UK IODP Phase 2 Moratorium Award [NE/P020909/1]. Conflict of Interest Statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Acknowledgments We thank Madalina Jaggi for laboratory support. PS thanks the Laboratoire d'Excellence LabexMER (ANR-10-LABX-19) and the GPI Laboratories, Inc. (Grand Rapids, MI, USA) for funding and analyses. OS thanks IODP-France for funding.",
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T1 - Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin

AU - Eickenbusch, Philip

AU - Takai, Ken

AU - Sissman, Olivier

AU - Suzuki, Shino

AU - Menzies, Catriona

AU - Sakai, Sanae

AU - Sansjofre, Pierre

AU - Tasumi, Eiji

AU - Bernasconi, Stefano M.

AU - Glombitza, Clemens

AU - Jørgensen, Bo Barker

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N1 - Funding This research used samples and/or data provided by the International Ocean Discovery Program (IODP). Additional support for the participation in IODP Expedition came from SwissDrilling (www.swissdrilling.ch), which is funded by the Swiss National Science Foundation (SNSF; www.snf.ch) project No. 182091 and by the Deep Carbon Observatory (www.deepcarbon.net). Funding for this research was provided by ETH Zurich. CG and BJ were supported by the Danish National Research Foundation [DNRF104], the European Research Council [ERC Advanced Grant #294200], and the Danish Council for Independent Research [DFF−7014-00196]. CM was supported by a NERC UK IODP Phase 2 Moratorium Award [NE/P020909/1]. Conflict of Interest Statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Acknowledgments We thank Madalina Jaggi for laboratory support. PS thanks the Laboratoire d'Excellence LabexMER (ANR-10-LABX-19) and the GPI Laboratories, Inc. (Grand Rapids, MI, USA) for funding and analyses. OS thanks IODP-France for funding.

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N2 - Serpentinitic systems are potential habitats for microbial life due to frequently high concentrations of microbial energy substrates, such as hydrogen (H2), methane (CH4), and short-chain organic acids (SCOAs). Yet, many serpentinitic systems are also physiologically challenging environments due to highly alkaline conditions (pH > 10) and elevated temperatures (>80.C). To elucidate the possibility of microbial life in deep serpentinitic crustal environments, International Ocean Discovery Program (IODP) Expedition 366 drilled into the Yinazao, Fantangisna, and Asut Tesoru serpentinite mud volcanoes on the Mariana Forearc. These mud volcanoes differ in temperature (80, 150, 250.C, respectively) of the underlying subducting slab, and in the porewater pH (11.0, 11.2, 12.5, respectively) of the serpentinite mud. Increases in formate and acetate concentrations across the three mud volcanoes, which are positively correlated with temperature in the subducting slab and coincide with strong increases in H2 concentrations, indicate a serpentinization-related origin. Thermodynamic calculations suggest that formate is produced by equilibrium reactions with dissolved inorganic carbon (DIC) + H2, and that equilibration continues during fluid ascent at temperatures below 80.C. By contrast, the mechanism(s) of acetate production are not clear. Besides formate, acetate, and H2 data, we present concentrations of other SCOAs, methane, carbon monoxide, and sulfate, d13C-data on bulk carbon pools, and microbial cell counts. Even though calculations indicate a wide range of microbial catabolic reactions to be thermodynamically favorable, concentration profiles of potential energy substrates, and very low cell numbers suggest that microbial life is scarce or absent. We discuss the potential roles of temperature, pH, pressure, and dispersal in limiting the occurrence of microbial life in deep serpentinitic environments.

AB - Serpentinitic systems are potential habitats for microbial life due to frequently high concentrations of microbial energy substrates, such as hydrogen (H2), methane (CH4), and short-chain organic acids (SCOAs). Yet, many serpentinitic systems are also physiologically challenging environments due to highly alkaline conditions (pH > 10) and elevated temperatures (>80.C). To elucidate the possibility of microbial life in deep serpentinitic crustal environments, International Ocean Discovery Program (IODP) Expedition 366 drilled into the Yinazao, Fantangisna, and Asut Tesoru serpentinite mud volcanoes on the Mariana Forearc. These mud volcanoes differ in temperature (80, 150, 250.C, respectively) of the underlying subducting slab, and in the porewater pH (11.0, 11.2, 12.5, respectively) of the serpentinite mud. Increases in formate and acetate concentrations across the three mud volcanoes, which are positively correlated with temperature in the subducting slab and coincide with strong increases in H2 concentrations, indicate a serpentinization-related origin. Thermodynamic calculations suggest that formate is produced by equilibrium reactions with dissolved inorganic carbon (DIC) + H2, and that equilibration continues during fluid ascent at temperatures below 80.C. By contrast, the mechanism(s) of acetate production are not clear. Besides formate, acetate, and H2 data, we present concentrations of other SCOAs, methane, carbon monoxide, and sulfate, d13C-data on bulk carbon pools, and microbial cell counts. Even though calculations indicate a wide range of microbial catabolic reactions to be thermodynamically favorable, concentration profiles of potential energy substrates, and very low cell numbers suggest that microbial life is scarce or absent. We discuss the potential roles of temperature, pH, pressure, and dispersal in limiting the occurrence of microbial life in deep serpentinitic environments.

KW - Abiotic synthesis

KW - Acetate

KW - Deep biosphere

KW - Formate

KW - International ocean discovery program

KW - Limits of life

KW - Methane

KW - Serpentinization

KW - deep biosphere

KW - HYDROGEN GENERATION

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KW - formate

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KW - REDUCING BACTERIA

KW - limits of life

KW - International Ocean Discovery Program

KW - VOLATILE FATTY-ACIDS

KW - DEEP SUBSEAFLOOR SEDIMENTS

KW - HYDROTHERMAL REACTIVITY

KW - serpentinization

KW - abiotic synthesis

KW - methane

KW - THERMOCHEMICAL SULFATE REDUCTION

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