Isotopic evidence of acetate turnover in Precambrian continental fracture fluids.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
23 Oct 2024
23 Oct 2024
Historique:
received:
30
12
2023
accepted:
08
10
2024
medline:
24
10
2024
pubmed:
24
10
2024
entrez:
23
10
2024
Statut:
epublish
Résumé
The deep continental crust represents a vast potential habitat for microbial life where its activity remains poorly constrained. Organic acids like acetate are common in these ecosystems, but their role in the subsurface carbon cycle - including the mechanism and rate of their turnover - is still unclear. Here, we develop an isotope-exchange 'clock' based on the abiotic equilibration of H-isotopes between acetate and water, which can be used to define the maximum in situ acetate residence time. We apply this technique to the fracture fluids in Birchtree and Kidd Creek mines within the Canadian Precambrian crust. At both sites, we find that acetate residence times are <1 million years and calculated a rate of turnover that could theoretically support microbial life. However, radiolytic water-rock reactions could also contribute to acetate production and degradation, a process that would have global relevance for the deep biosphere. More broadly, our study demonstrates the utility of isotope-exchange clocks in determining residence times of biomolecules with possible applications to other environments.
Identifiants
pubmed: 39443486
doi: 10.1038/s41467-024-53438-4
pii: 10.1038/s41467-024-53438-4
doi:
Substances chimiques
Acetates
0
Isotopes
0
Water
059QF0KO0R
Carbon Isotopes
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9130Subventions
Organisme : National Science Foundation (NSF)
ID : DGE-1745301
Organisme : NASA | NASA Astrobiology Institute (NAI)
ID : 80NSSC18M0094
Informations de copyright
© 2024. The Author(s).
Références
Ferguson, G. et al. Crustal groundwater volumes greater than previously thought. Geophys. Res. Lett. 48, e2021GL093549 (2021).
Bomberg, M. et al. Microbial metabolic potential in deep crystalline bedrock. 41–70 (Elsevier, 2021).
Holland, G. et al. Deep fracture fluids isolated in the crust since the Precambrian era. Nature 497, 357–360 (2013).
pubmed: 23676753
doi: 10.1038/nature12127
Lollar, G. S. et al. Follow the water’: hydrogeochemical constraints on microbial investigations 2.4 km below surface at the kidd creek deep fluid and deep life observatory. Geomicrobiol. J. 36, 859–872 (2019).
doi: 10.1080/01490451.2019.1641770
Lin, L.-H. et al. The yield and isotopic composition of radiolytic H
doi: 10.1016/j.gca.2004.07.032
Lin, L.-H. et al. Radiolytic H
doi: 10.1029/2004GC000907
Sherwood Lollar, B. et al. The contribution of the Precambrian continental lithosphere to global H
doi: 10.1038/nature14017
Nisson, D. M. et al. Hydrogeochemical and isotopic signatures elucidate deep subsurface hypersaline brine formation through radiolysis driven water-rock interaction. Geochim. Cosmochim. Acta 340, 65–84 (2023).
doi: 10.1016/j.gca.2022.11.015
Warr, O. et al. The application of Monte Carlo modelling to quantify in situ hydrogen and associated element production in the deep subsurface. Front. Earth Sci. 11, 1150740 (2023).
doi: 10.3389/feart.2023.1150740
Li, L. et al. Sulfur mass-independent fractionation in subsurface fracture waters indicates a long-standing sulfur cycle in Precambrian rocks. Nat. Commun. 7, 13252 (2016).
pubmed: 27807346
pmcid: 5095282
doi: 10.1038/ncomms13252
Sherwood Lollar, B. et al. Abiogenic methanogenesis in crystalline rocks. Geochim. Cosmochim. Acta 57, 5087–5097 (1993).
doi: 10.1016/0016-7037(93)90610-9
Etiope, G. & Sherwood Lollar, B. Abiotic methane on earth: abiotic methane on earth. Rev. Geophys. 51, 276–299 (2013).
doi: 10.1002/rog.20011
Taguchi, K. et al. Low 13C-13C abundances in abiotic ethane. Nat. Commun. 13, 5790 (2022).
pubmed: 36184637
pmcid: 9527245
doi: 10.1038/s41467-022-33538-9
Costagliola, A. et al. Radiolytic dissolution of calcite under gamma and helium ion irradiation. J. Phys. Chem. C 121, 24548–24556 (2017).
doi: 10.1021/acs.jpcc.7b07299
Vandenborre, J. et al. Carboxylate anion generation in aqueous solution from carbonate radiolysis, a potential route for abiotic organic acid synthesis on Earth and beyond. Earth Planet. Sci. Lett. 564, 116892 (2021).
doi: 10.1016/j.epsl.2021.116892
Sherwood Lollar, B. et al. A window into the abiotic carbon cycle – acetate and formate in fracture waters in 2.7 billion year-old host rocks of the Canadian Shield. Geochim. Cosmochim. Acta 294, 295–314 (2021).
doi: 10.1016/j.gca.2020.11.026
Templeton, A. S. & Caro, T. A. The rock-hosted biosphere. Annu. Rev. Earth Planet. Sci. 51, 493–519 (2023).
doi: 10.1146/annurev-earth-031920-081957
Warr, O. et al. The role of low-temperature
doi: 10.1016/j.chemgeo.2020.120027
Gao, J. A theoretical investigation of the enol content of acetic acid and the acetate ion in aqueous solution. J. Mol. Struct. Theochem. 370, 203–208 (1996).
doi: 10.1016/S0166-1280(96)04702-1
Mardyukov, A. et al. 1,1‐Ethenediol: the long elusive enol of acetic acid. Angew. Chem. Int. Ed. 59, 5577–5580 (2020).
doi: 10.1002/anie.201915646
Song, M., Warr, O., Telling, J. & Sherwood Lollar, B. Hydrogeological controls on microbial activity and habitability in the Precambrian continental crust. Geobiology 22, 12592 (2024).
doi: 10.1111/gbi.12592
Mueller, E. P. et al. Simultaneous, high-precision measurements of δ
pubmed: 34967622
doi: 10.1021/acs.analchem.1c04141
Magnabosco, C. et al. A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust. ISME J. 10, 730–741 (2016).
pubmed: 26325359
doi: 10.1038/ismej.2015.150
Jørgensen, B. B. et al. The biogeochemical sulfur cycle of marine sediments. Front. Microbiol. 10, 849 (2019).
pubmed: 31105660
pmcid: 6492693
doi: 10.3389/fmicb.2019.00849
Blair, N. E. & Carter, W. D. The carbon isotope biogeochemistry of acetate from a methanogenic marine sediment. Geochim. Cosmochim. Acta 56, 1247–1258 (1992).
doi: 10.1016/0016-7037(92)90060-V
Tijhuis, L. et al. A thermodynamically based correlation for maintenance gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnol. Bioeng. 42, 509–519 (1993).
pubmed: 18613056
doi: 10.1002/bit.260420415
Tappe, W. et al. Maintenance energy demand and starvation recovery dynamics of Nitrosomonas europaea and Nitrobacter winogradskyi cultivated in a retentostat with complete biomass retention. Appl. Environ. Microbiol. 65, 2471–2477 (1999).
pubmed: 10347029
pmcid: 91364
doi: 10.1128/AEM.65.6.2471-2477.1999
Bradley, J. A. et al. Widespread energy limitation to life in global subseafloor sediments. Sci. Adv. 6, eaba0697 (2020).
pubmed: 32821818
pmcid: 7406382
doi: 10.1126/sciadv.aba0697
Telling, J. et al. Bioenergetic constraints on microbial hydrogen utilization in precambrian deep crustal fracture fluids. Geomicrobiol. J. 35, 108–119 (2018).
doi: 10.1080/01490451.2017.1333176
Van Bodegom, P. Microbial maintenance: a critical review on its quantification. Microb. Ecol. 53, 513–523 (2007).
pubmed: 17333428
pmcid: 1915598
doi: 10.1007/s00248-006-9049-5
Heuer, V. B. et al. The stable carbon isotope biogeochemistry of acetate and other dissolved carbon species in deep subseafloor sediments at the northern Cascadia Margin. Geochim. Cosmochim. Acta 73, 3323–3336 (2009).
doi: 10.1016/j.gca.2009.03.001
Thomas, R. B. Intramolecular Isotopic Variation in Acetate in Sediments and Wetland Soils. Ph.D. Thesis. (2008).
Gelwicks, J. T. et al. Carbon isotope effects associated with autotrophic acetogenesis. Org. Geochem. 14, 441–446 (1989).
pubmed: 11542159
doi: 10.1016/0146-6380(89)90009-0
Lever, M. A. et al. Acetogenesis in deep subseafloor sediments of the Juan de Fuca ridge flank: a synthesis of geochemical, thermodynamic, and gene-based evidence. Geomicrobiol. J. 27, 183–211 (2010).
doi: 10.1080/01490450903456681
Blaser, M. B. et al. Carbon isotope fractionation of 11 acetogenic strains grown on H
pubmed: 23275504
pmcid: 3592252
doi: 10.1128/AEM.03203-12
Wellmer, F.-W. et al. Carbon isotope geochemistry of archean carbonaceous horizons in the timmins area. Soc. Econ. Geol. 10, 441–456 (1999).
Warr, O. et al. High-resolution, long-term isotopic and isotopologue variation identifies the sources and sinks of methane in a deep subsurface carbon cycle. Geochim. Cosmochim. Acta 294, 315–334 (2021).
doi: 10.1016/j.gca.2020.12.002
Heuer, V. et al. Online δ
doi: 10.4319/lom.2006.4.346
Gelwicks, J. T., Risatti, J. B. & Hayes, J. M. Carbon isotope effects associated with aceticlastic methanogenesis. Appl. Environ. Microbiol. 60, 467–472 (1994).
pubmed: 11536629
pmcid: 201335
doi: 10.1128/aem.60.2.467-472.1994
Wilpiszeski, R. L., Sherwood Lollar, B., Warr, O. & House, C. H. In situ growth of halophilic bacteria in saline fracture fluids from 2.4 km below surface in the deep canadian shield. Life 10, 307 (2020).
pubmed: 33255232
pmcid: 7760289
doi: 10.3390/life10120307
Beulig, F. et al. Control on rate and pathway of anaerobic organic carbon degradation in the seabed. Proc. Natl Acad. Sci. USA 115, 367–372 (2018).
pubmed: 29279408
doi: 10.1073/pnas.1715789115
Ouellette, R. J. & Rawn, J. D. Condensation reactions of carbonyl compounds. Org. Chem. 419–422 (2014).
Sessions, A. L. et al. Isotopic exchange of carbon-bound hydrogen over geologic timescales. Geochim. Cosmochim. Acta 68, 1545–1559 (2004).
doi: 10.1016/j.gca.2003.06.004
Hilkert, A. et al. Exploring the potential of electrospray-orbitrap for stable isootpe analysis using nitrate as a model. Anal. Chem. 26, 9139–9148 (2020).
Stephens, P. J. et al. Ab initio calculation of vibrational absorption and circular dichroism spectra using density functional force fields. J. Phys. Chem. 98, 11623–11627 (1994).
doi: 10.1021/j100096a001
Lee, C. et al. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 37, 785–789 (1988).
doi: 10.1103/PhysRevB.37.785
Urey, H. C. The thermodynamic properties of isotopic substances. J. Chem. Soc. 562–581 https://doi.org/10.1039/jr9470000562 (1947).
Wang, Y. et al. Equilibrium
doi: 10.1016/j.gca.2009.08.019
Miertuš, S., Scrocco, E. & Tomasi, J. Electrostatic interaction of a solute with a continuum. A direct utilizaion of AB initio molecular potentials for the prevision of solvent effects. Chem. Phys. 55, 117–129 (1981).
doi: 10.1016/0301-0104(81)85090-2
Miertus, S. & Tomasi, J. Approximate evaluations of the electrostatic free energy and internal energy changes in solution processes. Chem. Phys. 65, 239–245 (1982).
doi: 10.1016/0301-0104(82)85072-6
Muñoz Noval, Á., Nishio, D., Kuruma, T. & Hayakawa, S. Coordination and structure of Ca(II)-acetate complexes in aqueous solution studied by a combination of Raman and XAFS spectroscopies. J. Mol. Struct. 1161, 512–518 (2018).
doi: 10.1016/j.molstruc.2018.02.075
Horita, J., Wesolowski, D. J. & Cole, D. R. The activity-composition relationship of oxygen and hydrogen isotopes in aqueous salt solutions: I. Vapor-liquid water equilibration of single salt solutions from 50 to 100 °C. Geochim. Cosmochim. Acta 57, 2797–2817 (1993).
doi: 10.1016/0016-7037(93)90391-9
Mueller, E. elliottmueller/Mueller-2024-Data: Data Repository for Mueller et al. (2024) (v1.1). Zenodo. https://doi.org/10.5281/zenodo.13798759 (2024).