Abstract
Dissolved organic carbon (DOC) derived from thermokarst lakes is usually considered to be prone to microbial degradation and releases substantial carbon dioxide to the atmosphere, potentially enhancing the positive permafrost carbon (C)-climate feedback. In contrast to this long-term standing view, here we show that dark C fixation exceeds DOC degradation in ~1/3 of the investigated thermokarst lakes on the Tibetan Plateau, based on the combination of large-scale water and sediment sampling across seasons and years, biodegradable DOC experiments and 14C-labeling bicarbonate (NaH14CO3) assimilation incubation experiment. By employing qPCR, amplicon sequencing and metagenomic analyses, we find that microbial C fixation is mainly driven by nitrifying microorganisms via the Calvin-Benson-Bassham cycle carried out by the cbbL gene (encoding form I ribulose-1,5-bisphosphate carboxylase/oxygenase). These findings demonstrate that chemoautotrophic C fixation predominates in part of thermokarst lakes, which could partly offset C emissions upon permafrost thaw and thus weaken the positive permafrost C-climate feedback.
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Data availability
All data supporting the findings in this study are available in the figshare database (https://doi.org/10.6084/m9.figshare.30081886.v3)82 and Supplementary Information. The sequence data generated in this study have been deposited in the NCBI Sequence Read Archive (SRA) database under accession number PRJNA1363675. Source data are provided with this paper.
References
Abbott, B. W., Jones, J. B., Godsey, S. E., Larouche, J. R. & Bowden, W. B. Patterns and persistence of hydrologic carbon and nutrient export from collapsing upland permafrost. Biogeosciences 12, 3725–3740 (2015).
Olefeldt, D. et al. Circumpolar distribution and carbon storage of thermokarst landscapes. Nat. Commun. 7, 13043 (2016).
Wang, X. et al. Contrasting characteristics, changes, and linkages of permafrost between the Arctic and the Third Pole. Earth Sci. Rev. 230, 104042 (2022).
Turetsky, M. R. et al. Permafrost collapse is accelerating carbon release. Nature 569, 32–34 (2019).
Walter Anthony, K. et al. 21st-century modeled permafrost carbon emissions accelerated by abrupt thaw beneath lakes. Nat. Commun. 9, 3262 (2018).
Wik, M., Varner, R. K., Anthony, K. W., Macintyre, S. & Bastviken, D. Climate-sensitive northern lakes and ponds are critical components of methane release. Nat. Geosci. 9, 99–105 (2016).
Yang, G. et al. Characteristics of methane emissions from alpine thermokarst lakes on the Tibetan Plateau. Nat. Commun. 14, 3121 (2023).
Payandi-Rolland, D. et al. Dissolved organic matter biodegradation along a hydrological continuum in permafrost peatlands. Sci. Total Environ. 749, 141463 (2020).
Schuur, E. A. G. & Mack, M. C. Ecological response to permafrost thaw and consequences for local and global ecosystem services. Annu. Rev. Ecol. Evol. Syst. 49, 279–301 (2018).
Li, Z. et al. Accelerated organic matter decomposition in thermokarst lakes upon carbon and phosphorus inputs. Glob. Change Biol. 29, 6367–6382 (2023).
Vonk, J. E. et al. Biodegradability of dissolved organic carbon in permafrost soils and aquatic systems: a meta-analysis. Biogeosciences 12, 6915–6930 (2015).
Abbott, B. W., Larouche, J. R., Jones, J. B., Bowden, W. B. & Balser, A. W. Elevated dissolved organic carbon biodegradability from thawing and collapsing permafrost. J. Geophys. Res. Biogeosci. 119, 2049–2063 (2014).
Alfreider, A. et al. CO2 assimilation strategies in stratified lakes: diversity and distribution patterns of chemolithoautotrophs. Environ. Microbiol. 19, 2754–2768 (2017).
Cory, R. M., Crump, B. C., Dobkowski, J. A. & Kling, G. W. Surface exposure to sunlight stimulates CO2 release from permafrost soil carbon in the Arctic. Proc. Natl. Acad. Sci. USA 110, 3429–3434 (2013).
Cory, R. M., Ward, C. P., Crump, B. C. & Kling, G. W. Sunlight controls water column processing of carbon in arctic fresh waters. Science 345, 925–928 (2014).
Hu, J. et al. Photo-produced aromatic compounds stimulate microbial degradation of dissolved organic carbon in thermokarst lakes. Nat. Commun. 14, 3681 (2023).
Nalven, S. G. et al. Experimental metatranscriptomics reveals the costs and benefits of dissolved organic matter photo-alteration for freshwater microbes. Environ. Microbiol. 22, 3505–3521 (2020).
Raven, J. A. Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquat. Microb. Ecol. 56, 177–192 (2009).
Wei, Z. et al. Sentinel-based inventory of thermokarst lakes and ponds across permafrost landscapes on the Qinghai-Tibet Plateau. Earth Space Sci. 8, e2021EA001950 (2021).
Gao, T. et al. Accelerating permafrost collapse on the eastern Tibetan Plateau. Environ. Res. Lett. 16, 054023 (2021).
Vick-Majors, T. J. & Priscu, J. C. Inorganic carbon fixation in ice-covered lakes of the McMurdo Dry Valleys. Antarctic Sci. 31, 123–132 (2019).
Baltar, F., Arístegui, J., Gasol, J. M., Sintes, E. & Herndl, G. J. Evidence of prokaryotic metabolism on suspended particulate organic matter in the dark waters of the subtropical North Atlantic. Limnol. Oceanogr. 54, 182–193 (2009).
Dahlback, A., Gelsor, N., Stamnes, J. J. & Gjessing, Y. UV measurements in the 3000-5000 m altitude region in Tibet. J. Geophys. Res. 112, D09308 (2007).
Wickland, K. P. et al. Biodegradability of dissolved organic carbon in the Yukon River and its tributaries: seasonality and importance of inorganic nitrogen. Glob. Biogeochem. Cycles 26, GB0E03 (2012).
Berg, C., Listmann, L., Vandieken, V., Vogts, A. & Jurgens, K. Chemoautotrophic growth of ammonia-oxidizing Thaumarchaeota enriched from a pelagic redox gradient in the Baltic Sea. Front. Microbiol. 5, 786 (2015).
Berg, I. A. et al. Autotrophic carbon fixation in archaea. Nat. Rev. Microbiol. 8, 447–460 (2010).
Yakimov, M. et al. Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea). ISME J. 5, 945–961 (2011).
Berg, I. A., Kockelkorn, D., Bucket, W. & Fuchs, G. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318, 1782–1786 (2007).
Yakimov, M. M., Cono, V. L. & Denaro, R. A first insight into the occurrence and expression of functional amoA and accA genes of autotrophic and ammonia-oxidizing bathypelagic Crenarchaeota of Tyrrhenian Sea. Deep Sea Res. II Top. Stud. Oceanogr. 56, 748–754 (2009).
Offre, P., Nicol, G. W. & Prosser, J. I. Community profiling and quantification of putative autotrophic thaumarchaeal communities in environmental samples. Environ. Microbiol. Rep. 3, 245–253 (2011).
Badger, M. R. & Bek, E. J. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J. Exp. Bot. 59, 1525–1541 (2008).
Urakawa, H. et al. Ammonia availability shapes the seasonal distribution and activity of archaeal and bacterial ammonia oxidizers in the Puget Sound Estuary. Limnol. Oceanogr. 59, 1321–1335 (2015).
Overholt, W. A. et al. Carbon fixation rates in groundwater similar to those in oligotrophic marine systems. Nat. Geosci. 15, 561–567 (2022).
Bochet, O. et al. Iron-oxidizer hotspots formed by intermittent oxic-anoxic fluid mixing in fractured rocks. Nat. Geosci. 13, 149–155 (2020).
Mardanov, A. V., Beletsky, A. V., Kadnikov, V. T., Slobodkin, A. I. & Ravin, N. V. Genome Analysis of thermosulfurimonas dismutans, the first thermophilic sulfur-disproportionating bacterium of the phylum thermodesulfobacteria. Front. Microbiol. 7, 950 (2016).
Wasmund, K., Mumann, M. & Loy, A. The life sulfuric: microbial ecology of sulfur cycling in marine sediments. Environ. Microbiol. Rep. 9, 323–344 (2017).
Ding, J. et al. The permafrost carbon inventory on the Tibetan Plateau: a new evaluation using deep sediment cores. Glob. Change Biol. 22, 2688–2701 (2016).
Wang, T. et al. Permafrost thawing puts the frozen carbon at risk over the Tibetan Plateau. Sci. Adv. 6, eaaz3513 (2020).
Wang, D. et al. A 1km resolution soil organic carbon dataset for frozen ground in the Third Pole. Earth Sys. Sci. Data 13, 3453–3465 (2021).
Chen, L. et al. Permafrost carbon cycle and its dynamics on the Tibetan Plateau. Sci. China Life Sci. 67, 1833–1848 (2024).
Editorial Committee for Vegetation Map of China. Vegetation Atlas of China (Science Press, 2001).
Zhang, J., Wang, J., Chen, W., Li, B. & Zhao, K. Vegetation of Xizang (Tibet) (Science Press, 1988).
Zhao, L. & Sheng, Y. Permafrost and its changes on the Qinghai-Tibetan Plateau (Science Press, 2019).
Bai, Y. et al. Heating up the roof of the world: tracing the impacts of in-situ warming on carbon cycle in alpine grasslands on the Tibetan Plateau. Nat. Sci. Rev. 12, nwae371 (2025).
Fu, Z. et al. Non-temperature environmental drivers modulate warming-induced 21st-century permafrost degradation on the Tibetan Plateau. Nat. Commun. 16, 7556 (2025).
Mu, M. et al. Thermokarst lake changes along the Qinghai-Tibet Highway during 1991-2020. Geomorphology 441, 108895 (2023).
Kang, L. et al. Patterns and drivers of prokaryotic communities in thermokarst lake water across Northern Hemisphere. Glob. Ecol. Biogeogr. 32, 2244–2256 (2023).
Santoro, A. L., Bastviken, D., Tranvik, L. & Enrich-Prast, A. Simultaneous measurements of dark carbon fixation and bacterial production in lake sediment. Limnol. Oceanogr. Methods 11, 298–303 (2013).
Dyksma, S., Bischof, K., Fuchs, B. M., Hoffmann, K. & Mumann, M. Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments. ISME J. 10, 1939–1953 (2016).
Tolli, J. & King, G. M. Diversity and structure of bacterial chemolithotrophic communities in pine forest and agroecosystem soils. Appl. Environ. Microbiol. 71, 8411–8418 (2005).
Alfreider, A., Vogt, C., Hoffmannw, D. & Babel, W. Diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes from groundwater and aquifer microorganisms. Microb. Ecol. 45, 317–328 (2003).
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
Magoč, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).
Fish, J. et al. FunGene: the functional gene pipeline and repository. Front. Microbiol. 4, 1–14 (2013).
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – Approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).
Kang, L. et al. Metagenomic insights into microbial community structure and metabolism in alpine permafrost on the Tibetan Plateau. Nat. Commun. 15, 5920 (2024).
Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).
Dinghua, L., Chi-Man, L., Ruibang, L., Kunihiko, S. & Tak-Wah, L. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).
Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 11, 119 (2010).
Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
Cantalapiedra, C. P., Ana, H.-P., Ivica, L., Peer, B. & Jaime, H. C. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol. 38, 5825–5829 (2021).
Uritskiy, G. V., Jocelyne, D. R. & James, T. MetaWRAP-a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome 6, 158 (2018).
Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864–2868 (2017).
Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).
Aroney, S. T. N. et al. CoverM: read alignment statistics for metagenomics. Bioinformatics 41, p1 (2025).
Chaumeil, P. A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36, 1925–1927 (2019).
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, 256–259 (2019).
Zhou, Z. et al. METABOLIC: high-throughput profiling of microbial genomes for functional traits, metabolism, biogeochemistry, and community-scale functional networks. Microbiome 10, 33 (2022).
Mcilvin, M. R. & Altabet, M. A. Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Anal. Chem. 77, 5589–5595 (2005).
Anastácio, A. S., Harris, B., Yoo, H. I., Fabris, J. D. & Stucki, J. W. Limitations of the ferrozine method for quantitative assay of mineral systems for ferrous and total iron. Geochim. Cosmochim. Acta 72, 5001–5008 (2008).
Zopfi, J., Ferdelman, T. G. & Fossing, H. Distribution and fate of sulfur intermediates-sulfite, tetrathionate, thiosulfate, and elemental sulfur-in marine sediments. Geol. Soc. Am. 379, 97–116 (2004).
Drake, T. W., Wickland, K. P., Spencer, R. G., Mcknight, D. M. & Striegl, R. G. Ancient low-molecular-weight organic acids in permafrost fuel rapid carbon dioxide production upon thaw. Proc. Natl. Acad. Sci. USA 112, 13946–13951 (2015).
Weishaar, J. L. et al. Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Environ. Sci. Technol. 37, 4702–4708 (2003).
Helms, J. R. et al. Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter. Limnol. Oceanogr. 55, 955–969 (2008).
Ohno, T. Fluorescence inner-filtering correction for determining the humification index of dissolved organic matter. Environ. Sci. Technol. 36, 742–746 (2002).
Murphy, K. R., Stedmon, C. A., Graeber, D. & Bro, R. Fluorescence spectroscopy and multi-way techniques. PARAFAC. Anal. Methods 5, 6557–6566 (2013).
Fellman, J. B., Hood, E. & Spencer, R. G. M. Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics in freshwater ecosystems: a review. Limnol. Oceanogr. 55, 2452–2462 (2010).
R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing. (2022).
Liu, F. et al. Chemoautotrophic carbon fixation in thermokarst lakes on the Tibetan Plateau. Figshare https://doi.org/10.6084/m9.figshare.30081886.v3 (2025).
Zou, D., Zhao, L., Sheng, Y., Chen, J. & Cheng, G. A new map of permafrost distribution on the Tibetan Plateau. Cryosphere 11, 2527–2542 (2017).
Acknowledgements
The authors would like to thank the Isotope Laboratory Platform from the Institute of Biophysics, Chinese Academy of Sciences, and the Analytical and Testing Center of Beijing Normal University for supporting NaH14CO3 assimilation experiment. The authors would also be grateful to Drs. Hongjie Zhang (from Chinese Academy of Sciences), Guohua Jiang and Jianhua Huang (both are from Beijing Normal University) for their technical assistance with the isotopic analyses. This work was supported by the National Natural Science Foundation of China (32588202, 32425004, and 32571870), the National Key Research and Development Program of China (2022YFF0801903), the New Cornerstone Science Foundation through the XPLORER PRIZE, and the Fundamental Research Funds of the Chinese Academy of Forestry (CAFYBB2023QA004 and CAFYBB2024ZA034).
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Y.Y. conceived the idea. Y.Y., F.L., and L.K. designed the study. L.K., Z.L., F.L., W.Z., W.X., and X.L. conducted the field water and sediment sampling. F.L., L.K., Z.L., and W.X. performed the experiments. F.L. and L.K. analyzed the data. F.L., Y.Y., and L.K. wrote the manuscript with input from Z.L., J.P., B.W.A., L.C., S.Q., D.Z., and Y.P.
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Liu, F., Kang, L., Li, Z. et al. Chemoautotrophic carbon fixation in thermokarst lakes on the Tibetan Plateau.
Nat Commun (2025). https://doi.org/10.1038/s41467-025-67478-x
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DOI: https://doi.org/10.1038/s41467-025-67478-x
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