Deeply-sourced formate fuels sulfate reducers but not methanogens at Lost City hydrothermal field

Stefano M. Bernasconi,Julia M. McGonigle,Susan Q. Lang,Matthew O. Schrenk,Gretchen L. Früh-Green,William J. Brazelton

doi:10.1038/s41598-017-19002-5

Stefano M. Bernasconi, Julia M. McGonigle + Show 4 more

Open Access

https://doi.org/10.1038/s41598-017-19002-5

Copy DOI

Abstract

Hydrogen produced during water-rock serpentinization reactions can drive the synthesis of organic compounds both biotically and abiotically. We investigated abiotic carbon production and microbial metabolic pathways at the high energy but low diversity serpentinite-hosted Lost City hydrothermal field. Compound-specific 14C data demonstrates that formate is mantle-derived and abiotic in some locations and has an additional, seawater-derived component in others. Lipids produced by the dominant member of the archaeal community, the Lost City Methanosarcinales, largely lack 14C, but metagenomic evidence suggests they cannot use formate for methanogenesis. Instead, sulfate-reducing bacteria may be the primary consumers of formate in Lost City chimneys. Paradoxically, the archaeal phylotype that numerically dominates the chimney microbial communities appears ill suited to live in pure hydrothermal fluids without the co-occurrence of organisms that can liberate CO2. Considering the lack of dissolved inorganic carbon in such systems, the ability to utilize formate may be a key trait for survival in pristine serpentinite-hosted environments.

Highlights

Deep sea hydrothermal systems have long been recognized as important zones of biological activity in the anoxic subsurface, and as potential locations for the evolution of early life on Earth[1,2]
The Lost City Hydrothermal Field is an iconic example of a low-temperature serpentinization system, and fluids there have elevated formate concentrations (36–158 μM) that have been proposed to form abiotically, through equilibration[14]: HCO3− + H2 = HCOO− + H2O
The isotopic signature (13C, 14C) of formate was determined for 6 fluid samples collected from Lost City chimneys at 4 locations (Markers 2, C, B, 3; Fig. 1, Table 1 and Supplemental Table 1)

Summary

Results and Discussion

The isotopic signature (13C, 14C) of formate was determined for 6 fluid samples collected from Lost City chimneys at 4 locations (Markers 2, C, B, 3; Fig. 1, Table 1 and Supplemental Table 1). Mantle CO2 is 14C-free but multiple lines of evidence indicate it is stripped from fluids in the subsurface: (a) similar to other alkaline serpentinization systems[15], Lost City endmember fluids lack significant concentrations of any ∑CO2 (0.1–0.6 μmol/L, with the exception of Marker 3 where seawater inputs raise concentrations to 10–26 μmol/L; Table 1)[13] due to the rapid precipitation of calcium carbonate in the subsurface[22,33] (b) calcium carbonate from actively venting chimneys has modern 14C signatures, indicating that it is precipitated from seawater bicarbonate, and that mantle CO2 is not available (Table 1)[21,23,30]. Best Match ANME-2 metagenome (CAI64341.1) Desulfitibacter alkalitolerans (WP_028308877.1) Methylophaga muralis (WP_069296139.1) ANME-2 metagenome (CAI64341.1) Desulfitibacter alkalitolerans (WP_028308876.1) Desulfotalea pyschrophila (WP_041277585.1) Thalassobius mediterraneus (WP_058317529.1)

Identities Metagenome Coverage

Materials and Methods

Additional Information