Bioenergetic characterization of a shallow-sea hydrothermal vent system: Milos Island, Greece.

Shallow-sea hydrothermal systems, like their deep-sea and terrestrial counterparts, can serve as relatively accessible portals into the microbial ecology of subsurface environments. In this study, we determined the chemical composition of 47 sediment porewater samples along a transect from a diffuse...

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Main Authors: Guang-Sin Lu, Douglas E LaRowe, David A Fike, Gregory K Druschel, William P Gilhooly, Roy E Price, Jan P Amend
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0234175
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author Guang-Sin Lu
Douglas E LaRowe
David A Fike
Gregory K Druschel
William P Gilhooly
Roy E Price
Jan P Amend
author_facet Guang-Sin Lu
Douglas E LaRowe
David A Fike
Gregory K Druschel
William P Gilhooly
Roy E Price
Jan P Amend
author_sort Guang-Sin Lu
collection DOAJ
description Shallow-sea hydrothermal systems, like their deep-sea and terrestrial counterparts, can serve as relatively accessible portals into the microbial ecology of subsurface environments. In this study, we determined the chemical composition of 47 sediment porewater samples along a transect from a diffuse shallow-sea hydrothermal vent to a non-thermal background area in Paleochori Bay, Milos Island, Greece. These geochemical data were combined with thermodynamic calculations to quantify potential sources of energy that may support in situ chemolithotrophy. The Gibbs energies (ΔGr) of 730 redox reactions involving 23 inorganic H-, O-, C-, N-, S-, Fe-, Mn-, and As-bearing compounds were calculated. Of these reactions, 379 were exergonic at one or more sampling locations. The greatest energy yields were from anaerobic CO oxidation with NO2- (-136 to -162 kJ/mol e-), followed by reactions in which the electron acceptor/donor pairs were O2/CO, NO3-/CO, and NO2-/H2S. When expressed as energy densities (where the concentration of the limiting reactant is taken into account), a different set of redox reactions are the most exergonic: in sediments affected by hydrothermal input, sulfide oxidation with a range of electron acceptors or nitrite reduction with different electron donors provide 85~245 J per kg of sediment, whereas in sediments less affected or unaffected by hydrothermal input, various S0 oxidation reactions and aerobic respiration reactions with several different electron donors are most energy-yielding (80~95 J per kg of sediment). A model that considers seawater mixing with hydrothermal fluids revealed that there is up to ~50 times more energy available for microorganisms that can use S0 or H2S as electron donors and NO2- or O2 as electron acceptors compared to other reactions. In addition to revealing likely metabolic pathways in the near-surface and subsurface mixing zones, thermodynamic calculations like these can help guide novel microbial cultivation efforts to isolate new species.
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spelling doaj.art-cf3b2e9dea0a4868a5678f4f1a2e2fbd2022-12-21T22:37:08ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01156e023417510.1371/journal.pone.0234175Bioenergetic characterization of a shallow-sea hydrothermal vent system: Milos Island, Greece.Guang-Sin LuDouglas E LaRoweDavid A FikeGregory K DruschelWilliam P GilhoolyRoy E PriceJan P AmendShallow-sea hydrothermal systems, like their deep-sea and terrestrial counterparts, can serve as relatively accessible portals into the microbial ecology of subsurface environments. In this study, we determined the chemical composition of 47 sediment porewater samples along a transect from a diffuse shallow-sea hydrothermal vent to a non-thermal background area in Paleochori Bay, Milos Island, Greece. These geochemical data were combined with thermodynamic calculations to quantify potential sources of energy that may support in situ chemolithotrophy. The Gibbs energies (ΔGr) of 730 redox reactions involving 23 inorganic H-, O-, C-, N-, S-, Fe-, Mn-, and As-bearing compounds were calculated. Of these reactions, 379 were exergonic at one or more sampling locations. The greatest energy yields were from anaerobic CO oxidation with NO2- (-136 to -162 kJ/mol e-), followed by reactions in which the electron acceptor/donor pairs were O2/CO, NO3-/CO, and NO2-/H2S. When expressed as energy densities (where the concentration of the limiting reactant is taken into account), a different set of redox reactions are the most exergonic: in sediments affected by hydrothermal input, sulfide oxidation with a range of electron acceptors or nitrite reduction with different electron donors provide 85~245 J per kg of sediment, whereas in sediments less affected or unaffected by hydrothermal input, various S0 oxidation reactions and aerobic respiration reactions with several different electron donors are most energy-yielding (80~95 J per kg of sediment). A model that considers seawater mixing with hydrothermal fluids revealed that there is up to ~50 times more energy available for microorganisms that can use S0 or H2S as electron donors and NO2- or O2 as electron acceptors compared to other reactions. In addition to revealing likely metabolic pathways in the near-surface and subsurface mixing zones, thermodynamic calculations like these can help guide novel microbial cultivation efforts to isolate new species.https://doi.org/10.1371/journal.pone.0234175
spellingShingle Guang-Sin Lu
Douglas E LaRowe
David A Fike
Gregory K Druschel
William P Gilhooly
Roy E Price
Jan P Amend
Bioenergetic characterization of a shallow-sea hydrothermal vent system: Milos Island, Greece.
PLoS ONE
title Bioenergetic characterization of a shallow-sea hydrothermal vent system: Milos Island, Greece.
title_full Bioenergetic characterization of a shallow-sea hydrothermal vent system: Milos Island, Greece.
title_fullStr Bioenergetic characterization of a shallow-sea hydrothermal vent system: Milos Island, Greece.
title_full_unstemmed Bioenergetic characterization of a shallow-sea hydrothermal vent system: Milos Island, Greece.
title_short Bioenergetic characterization of a shallow-sea hydrothermal vent system: Milos Island, Greece.
title_sort bioenergetic characterization of a shallow sea hydrothermal vent system milos island greece
url https://doi.org/10.1371/journal.pone.0234175
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