TY - JOUR
T1 - Bioenergetic characterization of a shallow-sea hydrothermal vent system
T2 - Milos Island, Greece
AU - Lu, Guang Sin
AU - LaRowe, Douglas E.
AU - Fike, David A.
AU - Druschel, Gregory K.
AU - Gilhooly, William P.
AU - Price, Roy E.
AU - Amend, Jan P.
N1 - Publisher Copyright:
© 2020 Lu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2020/6
Y1 - 2020/6
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85086008410&partnerID=8YFLogxK
U2 - 10.1371/journal.pone.0234175
DO - 10.1371/journal.pone.0234175
M3 - Article
C2 - 32502166
AN - SCOPUS:85086008410
SN - 1932-6203
VL - 15
JO - PloS one
JF - PloS one
IS - 6
M1 - e0234175
ER -