Abstract
Hydrothermal vents release substantial amounts of ancient carbon into the ocean, primarily as carbon dioxide, yet the extent to which this carbon is integrated into marine food webs remains poorly constrained. Here, we present a combination of bulk radiocarbon and stable carbon isotope measurements of particulate organic carbon from water column filters with compound-specific hydrogen and radiocarbon isotope analyses of fatty acids from surface sediments to trace carbon assimilation across benthic and pelagic realms in a low pH, shallow-water hydrothermal system off Taiwan. Isotope correlations indicate that vent-derived carbon dioxide constitutes a substantial fraction of the local microbial and faunal biomass through chemoautotrophic pathways (up to ~30%). Farther from the vents, hydrothermal carbon remains detectable and is incorporated into photoautotrophic biomass in the overlying water column. Notably, ancient carbon content in the standing stock of particulate organic carbon was higher at the lower temperature (“White”) vent, even though fluid and sulfide emissions – and thus potential energy availability – were substantially greater at the higher temperature (“Yellow”) vent. These findings show that physicochemical conditions, including pH and temperature, rather than fluid chemistry alone, control carbon assimilation patterns and ultimately limit the retention of vent-derived carbon in this shallow-water system.
Similar content being viewed by others
Data availability
Compound-specific δ2H and Δ14C data, as well as bulk δ2Hwater and Δ14CPOC data, are reported within the supplementary material and are available at https://doi.org/10.5281/zenodo.18310623. Compound-specific δ13C data can be found in Ref. 28 and within the PANGAEA database (Maak et al.73).
Code availability
All Code necessary to understand the manuscript can be accessed in Code Ocean.
References
Pohlman, J. W., Bauer, J. E., Waite, W. F., Osburn, C. L. & Chapman, N. R. Methane hydrate-bearing seeps as a source of aged dissolved organic carbon to the oceans. Nat. Geosci. 4, 37–41 (2011).
Wang, X.-C., Chen, R. F., Whelan, J. & Eglinton, L. Contribution of “old” carbon from natural marine hydrocarbon seeps to sedimentary and dissolved organic carbon pools in the Gulf of Mexico. Geophys. Res. Lett. 28, 3313–3316 (2001).
McCarthy, M. D. et al. Chemosynthetic origin of 14C-depleted dissolved organic matter in a ridge-flank hydrothermal system. Nat. Geosci. 4, 32–36 (2011).
Gomez-Saez, G. V. et al. Molecular evidence for abiotic sulfurization of dissolved organic matter in marine shallow hydrothermal systems. Geochim. Cosmochim. Acta 190, 35–52 (2016).
Estes, E. R. et al. Abiotic synthesis of graphite in hydrothermal vents. Nat. Commun. 10, 5179 (2019).
Wang, S.-L., Lin, Y.-S., Burr, G. S., Wang, P.-L. & Lin, L.-H. Radiocarbon and stable carbon isotope constraints on the propagation of vent CO2 to fluid in the acidic Kueishantao shallow water hydrothermal system. Geochem. Geophys. 23, e2022GC010508 (2022).
Druffel, E. R. M. & Griffin, S. Radiocarbon in dissolved organic carbon of the South Pacific Ocean. Geophys. Res. Lett. 42, 4096–4101 (2015).
McNichol, J. et al. Genus-specific carbon fixation activity measurements reveal distinct responses to oxygen among hydrothermal vent Campylobacteria. Appl. Environ. Microbiol. 88, e02083–21 (2022).
Sievert, S. et al. Fluid flow stimulates chemoautotrophy in hydrothermally influenced coastal sediments. Commun. Earth Environ. 3, 96 (2022).
Deng, W. et al. Strategies of chemolithoautotrophs adapting to high temperature and extremely acidic conditions in a shallow hydrothermal ecosystem. Microbiome 11, 270 (2023).
Achberger, A. M. et al. Inactive hydrothermal vent microbial communities are important contributors to deep ocean primary productivity. Nat. Microbiol. 9, 657–668 (2024).
Wegener, G. et al. Hydrothermal vents supporting persistent plumes and microbial chemoautotrophy at Gakkel Ridge (Arctic Ocean). Front. Microbiol. 15, 1473822 (2024).
Chen, C.-T. A. et al. Investigation into extremely acidic hydrothermal fluids off Kueishan Tao, Taiwan, China. Acta Oceanol. Sin. 24, 125–133 (2005).
Chen, C.-T. A. et al. Tide-influenced acidic hydrothermal system offshore NE Taiwan. Chem. Geol. 224, 69–81 (2005).
Lin, Y.-S. et al. Biogeochemistry and dynamics of particulate organic matter in a shallow-water hydrothermal field (Kueishantao Islet, NE Taiwan). Mar. Geol. 422, 106121 (2020).
Lin, Y.-S. et al. Fates of vent CO2 and its impact on carbonate chemistry in the shallow-water hydrothermal field offshore Kueishantao Islet, NE Taiwan. Mar. Chem. 210, 1–12 (2019).
Waite, D. W. et al. Comparative genomic analysis of the class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. nov.). Front. Microbiol. 8, 682 (2017).
Zhang, Y. et al. Sulfur-metabolizing microbes dominate microbial communities in andesite-hosted shallow-sea hydrothermal systems. PLOS ONE 7, e44593 (2012).
Wang, L., Cheung, M. K., Kwan, H. S., Hwang, J.-S. & Wong, C. K. Microbial diversity in shallow-water hydrothermal sediments of Kueishan Island, Taiwan as revealed by pyrosequencing. J. Basic Microbiol. 55, 1308–1318 (2015).
Tang, K., Liu, K., Jiao, N., Zhang, Y. & Chen, C.-T. A. Functional metagenomic investigations of microbial communities in a shallow-sea hydrothermal system. PLOS ONE 8, e72958 (2013).
Tang, K. et al. Cultivation-independent and cultivation-dependent analysis of microbes in the shallow-sea hydrothermal system off Kueishantao Island, Taiwan: Unmasking heterotrophic bacterial diversity and functional capacity. Front. Microbiol. 9, 279 (2018).
Lin, Y.-S. et al. Intense but variable autotrophic activity in a rapidly flushed shallow-water hydrothermal plume (Kueishantao Islet, Taiwan). Geobiology 19, 87–101 (2020).
Valentine, D. L. Isotopic remembrance of metabolism past. Proc. Natl. Acad. Sci. USA 106, 12565–12566 (2009).
Zhang, X., Gillespie, A. L. & Sessions, A. L. Large D/H variations in bacterial lipids reflect central metabolic pathways. Proc. Natl. Acad. Sci. USA 106, 12580–12586 (2009).
Osburn, M. R., Dawson, K. S., Fogel, M. L. & Sessions, A. L. Fractionation of hydrogen isotopes by sulfate- and nitrate-reducing bacteria. Front. Microbiol. 7, 627 (2016).
Hayes, J. Fractionation of carbon and hydrogen isotopes in biosynthetic processes. Rev. Mineral. Geochem. 43, 225–277 (2001).
House, C. H., Schopf, J. W. & Stetter, K. O. Carbon isotopic fractionation by Archaeans and other thermophilic prokaryotes. Org. Geochem. 34, 345–356 (2003).
Maak, J. M. et al. The energy-efficient reductive tricarboxylic acid cycle drives carbon uptake and transfer to higher trophic levels within the Kueishantao shallow-water hydrothermal system. Biogeosciences 22, 1853–1863 (2025).
Ruben, M. et al. Fossil organic carbon utilization in marine Arctic fjord sediments by subsurface micro-organisms. Nat. Geosci. 16, 625–630 (2023).
Campbell, B. J. & Cary, S. C. Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal vents. Appl. Environ. Microbiol. 70, 6282–6289 (2004).
Jónasdóttir, S. H. Fatty acid profiles and production in marine phytoplankton. Mar. Drugs 17, 151 (2019).
Ng, N., Huang, J. F. & Ho, P. H. Description of a new species of hydrothermal crab, Xenograpsus testudinatus (Crustacea: Decapoda: Brachyura: Grapsidae) from Taiwan. National Taiwan Museum Special Publication Series 10, 191–199 (2000).
Shanks, W. C. III & Seyfried, W. E. Jr Stable isotope studies of vent fluids and chimney minerals, southern Juan de Fuca Ridge: Sodium metasomatism and seawater sulfate reduction. J. Geophys. Res. Solid Earth 92, 11387–11399 (1987).
Chen, M., et al. Highly diverse diazotrophs drive high N2 fixation rates in a shallow submarine hydrothermal system. Fundam. Res. https://doi.org/10.1016/j.fmre.2023.07.009 (2023).
Chen, X.-G. et al. Heavy metals from Kueishantao shallow-sea hydrothermal vents, offshore northeast Taiwan. J. Mar. Syst. 180, 211–219 (2018).
Pichler, T., Veizer, J. & Hall, G. E. M. The chemical composition of shallow-water hydrothermal fluids in Tutum Bay, Ambitle Island, Papua New Guinea and their effect on ambient seawater. Mar. Chem. 64, 229–252 (1999).
Kao, S. J. et al. Preservation of terrestrial organic carbon in marine sediments offshore Taiwan: mountain building and atmospheric carbon dioxide sequestration. Earth Surf. Dynam. 2, 127–139 (2014).
Bao, R. et al. Widespread dispersal and aging of organic carbon in shallow marginal seas. Geology 44, 791–794 (2016).
Liang, W. D., Tang, T. Y., Yang, Y. J., Ko, M. T. & Chuang, W. S. Upper-ocean currents around Taiwan. Deep-Sea Res. II: Top. Stud. Oceanogr. 50, 1085–1105 (2003).
Hung, J. J., Yeh, H. Y., Peng, S. H. & Chen, C. T. A. Influence of submarine hydrothermalism on sulfur and metal accumulation in surface sediments in the Kueishantao venting field off northeastern Taiwan. Mar. Chem. 198, 88–96 (2018).
Wang, L. et al. Metagenomic insights into the functions of microbial communities in sulfur-rich sediment of a shallow-water hydrothermal vent off Kueishan Island. Front. Microbiol. 13, 992034 (2022).
Wu, J. Y. et al. Differential feeding habits of the shallow-water hydrothermal vent crab Xenograpsus testudinatus correlate with their resident vent types at a scale of meters. Biogeosciences 20, 2693–2706 (2023).
Mei, K. et al. Transformation, fluxes and impacts of dissolved metals from shallow water hydrothermal vents on nearby ecosystem offshore of Kueishantao (NE Taiwan). Sustainability 14, 1754 (2022).
Alberty, R. A. Calculating apparent equilibrium constants of enzyme-catalyzed reactions at pH 7. Biochem. Educ. 28, 12–17 (2000).
Thauer, R. K., Jungermann, K. & Decker, K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41, 100–180 (1977).
Inagaki, F., Takai, K., Kobayashi, H., Nealson, K. H. & Horikoshi, K. Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing ε-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int. J. Syst. Evol. Microbiol. 53, 1801–1805 (2003).
Inagaki, F., Takai, K., Nealson, K. H. & Horikoshi, K. Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the ε-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int. J. Syst. Evol. Microbiol. 54, 1477–1482 (2004).
Woulds, C., Bell, J. B., Glover, A. G., Bouillon, S. & Brown, L. S. Benthic carbon fixation and cycling in diffuse hydrothermal and background sediments in the Bransfield Strait, Antarctica. Biogeosciences 17, 1–12 (2020).
Reysenbach, A.-L. & Shock, E. Merging genomes with geochemistry in hydrothermal ecosystems. Science 296, 1077–1082 (2002).
Wang, L. et al. Diversity of total bacterial communities and chemoautotrophic populations in sulfur-rich sediments of shallow-water hydrothermal vents off Kueishan Island, Taiwan. Microb. Ecol. 73, 571–582 (2017).
Li, Y. et al. Coupled carbon, sulfur, and nitrogen cycles mediated by microorganisms in the water column of a shallow-water hydrothermal ecosystem. Front. Microbiol. 9, 2718 (2018).
Elling, F. J. et al. Marine and terrestrial nitrifying bacteria are sources of diverse bacteriohopanepolyols. Geobiology 20, 399–420 (2022).
Aepfler, R. F., Bühring, S. I. & Elvert, M. Substrate characteristic bacterial fatty acid production based on amino acid assimilation and transformation in marine sediments. FEMS Microbiol. Ecol. 95, fiz142 (2019).
Zhu, Q.-Z., Wegener, G., Hinrichs, K.-U. & Elvert, M. Activity of ancillary heterotrophic community members in anaerobic methane-oxidizing cultures. Front. Microbiol. 13, 892654 (2022).
Luther III, G. W. Hydrothermal vents are a source of old refractory organic carbon to the deep ocean. Geophys. Res. Lett. 48, e2021GL094869 (2021).
Valentine, D. L., Sessions, A. L., Tyler, S. C. & Chidthaisong, A. Hydrogen isotope fractionation during H2/CO2 acetogenesis: hydrogen utilization efficiency and the origin of lipid-bound hydrogen. Geobiology 2, 179–188 (2004).
Campbell, B. J., Li, C., Sessions, A. L. & Valentine, D. L. Hydrogen isotopic fractionation in lipid biosynthesis by H2-consuming Desulfobacterium autotrophicum. Geochim. Cosmochim. Acta 73, 2744–2757 (2009).
Heinzelmann, S. M. et al. Impact of metabolism and growth phase on the hydrogen isotopic composition of microbial fatty acids. Front. Microbiol. 6, 408 (2015).
Sessions, A. L., Caltech Fractome Database, California Institute of Technology (2015).
Zhang, Z., Sachs, J. P. & Marchetti, A. Hydrogen isotope fractionation in freshwater and marine algae: II. Temperature and nitrogen-limited growth rate effects. Org. Geochem. 40, 428–439 (2009).
Chen, X. et al. Impact of metabolism and temperature on 2H ∕ 1H fractionation in lipids of the marine bacterium Shewanella piezotolerans WP3. Biogeosciences 20, 1491–1504 (2023).
Onyenwoke, R. U. & Wiegel, J., Thermoanaerobacter, in Bergey’s Manual of Systematics of Archaea and Bacteria. p. 1–29. (2015).
Gomez-Saez, G. V. et al. Relative importance of chemoautotrophy for primary production in a light exposed marine shallow hydrothermal system. Front. Microbiol. 8, 35–52 (2017).
Chen, X.-G. et al. The chemical and isotopic compositions of gas discharge from shallow-water hydrothermal vents at Kueishantao, offshore northeast Taiwan. Geochem. J. 50, 341–355 (2016).
Takai, K. et al. Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int. J. Syst. Evol. Microbiol. 56, 1725–1733 (2006).
Sturt, H. F., Summons, R. E., Smith, K., Elvert, M. & Hinrichs, K.-U. Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry—new biomarkers for biogeochemistry and microbial ecology. Rapid Commun. Mass Spectrom. 18, 617–628 (2004).
Eglinton, T. I., Aluwihare, L. I., Bauer, J. E., Druffel, E. R. M. & McNichol, A. P. Gas chromatographic isolation of individual compounds from complex matrices for radiocarbon dating. Anal. Chem. 68, 904–912 (1996).
Mollenhauer, G., Grotheer, H., Gentz, T., Bonk, E. & Hefter, J. Standard operation procedures and performance of the MICADAS radiocarbon laboratory at Alfred Wegener Institute (AWI), Germany. Nucl. Instrum. Methods Phys. Res. B 496, 45–51 (2021).
Sun, S. et al. 14C blank assessment in small-scale compound-specific radiocarbon analysis of lipid biomarkers and lignin phenols. Radiocarbon 62, 207–218 (2020).
Winterfeld, M. et al. Deglacial mobilization of pre-aged terrestrial carbon from degrading permafrost. Nat. Commun. 9, 3666 (2018).
Druffel, E. R. M. et al. Marine organic carbon and radiocarbon- present and future challenges. Radiocarbon 64, 705–721 (2022).
D’Errico, J. inpaint_nans. MATLAB Central File Exchange. https://www.mathworks.com/matlabcentral/fileexchange/4551-inpaint_nans (2024).
Maak, J. M., et al., Fatty acid concentrations and compound-specific carbon stable isotopes of sediments, filtered particulate organic carbon, and crab tissue from the hydrothermal vent system off Kueishantao, Taiwan, https://doi.org/10.1594/PANGAEA.967575, PANGAEA (2025).
Acknowledgements
We express our gratitude to the Taiwan Ministry of Environment for granting permission to access the samples. Additionally, we extend our thanks to the scientists, crew members, and scientific divers who participated in the OR2−2024 and OR2−2095 cruises aboard the RV Ocean Researcher II, as well as those involved in the sampling conducted during a fishing boat expedition from May 25–28, 2015. We further thank Rebecca Aepfler (AWI, Bremerhaven) and Prof. Li-Lian Liu (National Sun Yat-sen University) for their help during sampling. This study was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy (EXC − 2077—390741603), a DFG Emmy Noether Grant awarded to S.I.B. (BU 2606/1−1), and the DAAD (Projektbezogener Personenaustausch − 57138084, awarded to S.I.B. and Y.-S.L.). We are grateful to the several anonymous reviewers for their time, careful reading, and constructive comments that helped improve the manuscript. We also acknowledge financial support for open-access publishing from the University of Bremen’s Open Access Publication Fund.
Funding
Open Access funding enabled and organized by Projekt DEAL.
Author information
Authors and Affiliations
Contributions
Joely Marie Maak: Conceptualization, data analysis, visualization, interpretation, writing—original draft, editing. Marcus Elvert: Conceptualization, supervision, review, editing. Hendrik Grotheer: Conceptualization, data analysis, interpretation, review, editing. Yu-Shih Lin: Sample collection, review, editing. Gesine Mollenhauer: Conceptualization, data analysis, review, editing. In-Tian Lin: Sample collection, interpretation, review, editing. Solveig I. Bühring: Conceptualization, supervision, review, editing. Enno Schefuß: Conceptualization, supervision, review, editing.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Communications Earth and Environment thanks Huei-Ting Lin and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editor: Alice Drinkwater. [A peer review file is available].
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Maak, J.M., Elvert, M., Grotheer, H. et al. Physicochemical controls on ancient carbon assimilation into ecosystem biomass in shallow-water hydrothermal systems. Commun Earth Environ (2026). https://doi.org/10.1038/s43247-026-03254-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s43247-026-03254-z


