Abstract
Lakes are hotspots for the biogeochemical processing of carbon, including dissolved organic matter (DOM). A less degradable fraction of DOM, preserved for a long time, can be categorized as recalcitrant DOM (RDOM). Lake RDOM is an important but neglected carbon sink, and its characteristics and transformation processes remain largely unknown.
Highlights
• Recalcitrant dissolved organic matter (RDOM) is an important but neglected carbon sink in lakes.
• The heterogeneity of lake environments determines the diversity and complexity of RDOM.
• New techniques allow detailed studies of the mechanisms of RDOM formation and related processes.
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1 Main text
The transport, transformation, production, degradation, and mineralization of organic carbon in inland ecosystems largely determine greenhouse gas emissions and the carbon balance, with implications for climate change (Battin et al. 2009). Despite that lakes cover < 2% of the Earth's surface area, they act as a fundamental link between the carbon cycles of terrestrial and inland water ecosystems. Globally, lakes and other wetland ecosystems fix organic carbon equivalent to ~ 50% of the organic carbon uptake by the oceans (Tranvik et al. 2009). Dissolved organic matter (DOM) typically constitutes the dominant pool of organic carbon in freshwaters (Drake et al. 2023; Zhou et al. 2023). Due to the differential degradation of DOM in lakes depending on bioavailability and photodegradability, the role of lakes in offsetting human CO2 emissions is uncertain (Jia et al. 2023). DOM preserved for a long period of time is categorized as recalcitrant DOM (RDOM), considered as a carbon sink (Xia et al. 2022). RDOM in the ocean can have a mean turnover time of about 5,000 years (Jiao et al. 2010); however, so far, the turnover time of RDOM in lakes is largely unknown.
In lake ecosystems, DOM is classified according to its sources (autochthonous or allochthonous) and its lability (highly labile, semi-labile, and recalcitrant) (Jiao et al. 2010). Degradation of algae and aquatic plants in lakes contributes to the production of autochthonous DOM (Zhang et al. 2009). Allochthonous DOM inputs mainly comprise DOM derived from soil leachate, domestic sewage, and agricultural effluents and they are typically major contributors to the lake DOM pool. These DOM inputs can undergo significant bacterial and UV transformation after entering a lake, with terrestrial aromatic DOM being selectively photodegraded to low-molecular-weight compounds and CO2 (Fig. 1; Cory et al. 2013). In pristine catchments, soil organic matter is the primary contributor to the allochthonous DOM pool and can be biologically stable (Drake et al. 2019). In comparison, autochthonous DOM derived from algal degradation produces most of the low-molecular-weight organic compounds, including amino acids, carbohydrates, and carboxylic acids, which can be readily utilized by microorganisms and degraded to dissolved inorganic matter and CO2 (Fig. 1). Therefore, autochthonous DOM is considered to be more biologically labile than soil-derived allochthonous DOM (Salcher et al. 2013). Due to the variations in lake environments and the associated biological communities and activities, the chemical composition and molecular structural stability of different DOM sources vary widely (Guillemette et al. 2015). For example, submerged plants have cellulose that is more difficult to degrade, and diatoms have a higher proportion of nondegradable glycine compared to cyanobacteria. However, the dynamics of RDOM in lakes are so far not well studied (Xia et al. 2022).
The turnover time of DOM in rivers and lakes is much shorter than in the ocean but cannot be directly estimated using the Δ14C dating technique (Xia et al. 2022). In streams, RDOM can contribute up to 62% of the total DOM pool (McLaughlin and Kaplan 2013). Microbial degradation experiments have shown that labile DOM in lake water accounts for up to > 50% of the DOM pool (Zhou et al. 2020) and that microorganisms would preferentially utilize freshly produced DOM, leaving RDOM for downstream discharge (Lu et al. 2013) or storage in the lakes (e.g., by flocculation followed by sedimentation). In addition to the imported allochthonous DOM, the metabolites, residues, and cell debris of primary production in lakes are relatively recalcitrant after utilization by microorganisms, and this RDOM fraction accounts, for example, for ~ 50% of the DOM pool in karst lakes (Xia et al. 2022). In closed catchments formed by impermeable bedrock in Antarctica fresh waters, autochthonous DOM forms ubiquitous and persistent in-water humus after photodegradation (Kida et al. 2019). Accordingly, it has been found that photooxidation of DOM constitutes 70%-95% of the total carbon processed in Arctic fresh waters (Cory et al. 2014). Photochemical processes have also been shown to enhance the cross-linking, humidification, and polymerization of unstable biomolecules into more recalcitrant compounds (Hassett 2006).
Most RDOM in lakes is the product of microbial metabolism. DOM serves as a major bacterial source of carbon and nutrients for metabolic activities. DOM aromaticity associating negatively with the bioavailability of organic matter can lead to differences in bacterial community structure, function, and mutualistic networks by affecting bacterial primary and secondary productivity, growth, and respiration rates (Guillemette et al. 2015; Hassett 2006; Zhou et al. 2021). Previous studies have shown that bacterial utilization of DOM is largely based on physiological needs but also influenced by environmental factors such as temperature, dissolved oxygen, and nutrient availability, which provide sufficient energy and materials for the synthesis of the necessary extracellular and transport enzymes (Xenopoulos et al. 2021). Environmental heterogeneity is a key factor in shaping the distribution patterns of planktonic bacteria in lakes and species richness (Zhou et al. 2021). Higher microbial diversity may provide more metabolic pathways to degrade and produce RDOM molecules (Zhou et al. 2021). Elucidating the chemical composition and quantifying the size of the RDOM pool are highly relevant to obtain carbon neutrality. Further disentangling the coupling linkages between environmental factors, bacterioplankton, and DOM is crucial for the understanding of the stability of carbon sources and sinks in lakes (Xia et al. 2022) and should be a future research priority.
There is a lack of hypotheses associated with the production and stability of RDOM in lake ecosystems. In comparison, reasons for the stability of RDOM in the oceans are currently summarized under the umbrella of three major hypotheses, the "environment hypothesis", the "intrinsic stability hypothesis", and the "molecular diversity hypothesis" (Dittmar 2015). The "environmental hypothesis" of RDOM production links DOM to the responsiveness of specific environmental conditions or to specific time periods (Dittmar 2015). These include the composition and activity of planktonic bacterial communities, redox state, mineral binding, and substrate accessibility by microorganisms and their enzymes. For example, limited availability of inorganic and organic nutrients may limit bacterial growth and DOM utilization through competition. Elucidating the key factors that influence the degradability and stability of DOM in lakes is an important area of future research. The "intrinsic stability hypothesis" links the reactivity of DOM to its molecular composition (Dittmar 2015). The molecular composition of RDOM may be synthesized by aquatic microbes, or it may be altered by abiotic modifications due to physicochemical perturbations. These abiotic modifications may result in the formation of a more stable fraction of DOM (Cory et al. 2014), thus contributing to the RDOM pool in lakes. The "molecular diversity hypothesis" suggests that bacteria in the deep ocean must maintain appropriate enzymes, transport systems, and metabolic pathways for DOM catabolism and anabolism (Dittmar 2015; Arrieta et al. 2015). However, such a strategy is difficult to have if the RDOM has a diverse chemical composition or the concentration is too low to be utilized by microbes. Due to the complexity of lake environments and the high biological activity in lakes, the composition of DOM and the stability of the molecular structure vary tremendously among different aquatic organisms in lakes. The "environmental hypothesis" mechanism may play an important role in the stability of DOM in lake ecosystems. Therefore, identifying the interactions between RDOM and planktonic bacteria across different environmental gradients (e.g., trophic status, catchment land use, sorption to metals and clay minerals) is key to understanding the dynamics of RDOM in lakes.
Fortunately, advances are made in metagenomic analysis and DOM identification, involving growing utilization of high- and ultrahigh-resolution mass spectrometry (e.g., FT-ICR MS and Orbitrap MS) (Hu et al. 2022). This provides unique opportunities to explore the link between microbial carbon pumps and the mechanisms of RDOM formation and to deepen our understanding of the interactions between the microbial community and the chemical composition of DOM as well as the outgassing of greenhouse gases from lakes (Li et al. 2022; McDonough et al. 2022). Big data and systems science approaches, including machine learning and numerical simulation, can further help to elucidate the role of RDOM in the lake carbon cycling and the role of lakes relative to the future climate change.
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Abbreviations
- CO2 :
-
Carbon dioxide
- DOM:
-
Dissolved organic matter
- FT-ICR MS:
-
Fourier transform ion cyclotron resonance mass spectrometry
- RDOM:
-
Recalcitrant dissolved organic matter
References
Arrieta JM, Mayol E, Hansman RL, Herndl GJ, Dittmar T, Duarte CM (2015) Dilution limits dissolved organic carbon utilization in the deep ocean. Science 348(6232):331–333
Battin TJ, Luyssaert S, Kaplan LA, Aufdenkampe AK, Richter A, Tranvik LJ (2009) The boundless carbon cycle. Nat Geosci 2(9):598–600. https://doi.org/10.1038/ngeo618
Cory RM, Crump BC, Dobkowski JA, Kling GW (2013) Surface exposure to sunlight stimulates CO2 release from permafrost soil carbon in the Arctic. Proc Natl Acad Sci USA 110(9):3429–3434. https://doi.org/10.1073/pnas.1214104110
Cory RM, Ward CP, Crump BC, Kling GW (2014) Sunlight controls water column processing of carbon in arctic fresh waters. Science 345(6199):925–928
Dittmar T (2015) Reasons behind the long-term stability of dissolved organic matter. Elsevier, In Biogeochemistry of marine dissolved organic matter, pp 369–388
Drake TW, Van Oost K, Barthel M, Bauters M, Hoyt AM, Podgorski DC, Six J, Boeckx P, Trumbore SE, Ntaboba LC et al (2019) Mobilization of aged and biolabile soil carbon by tropical deforestation. Nat Geosci 12(7):541–546. https://doi.org/10.1038/s41561-019-0384-9
Drake TW, Barthel M, Mbongo CE, Mpambi DM, Baumgartner S, Botefa CI, Bauters M, Kurek MR, Spencer RG, McKenna AM (2023) Hydrology drives export and composition of carbon in a pristine tropical river. Limnol Oceanogr 68(11):2476–2491
Guillemette F, Leigh McCallister S, Del Giorgio PA (2015) Selective consumption and metabolic allocation of terrestrial and algal carbon determine allochthony in lake bacteria. ISME J 10(6):1373–1382. https://doi.org/10.1038/ismej.2015.215
Hassett JP (2006) Chemistry. Dissolved natural organic matter as a microreactor. Science 311(5768):1723–1724. https://doi.org/10.1126/science.1123389
Hu X, Zhou Y, Zhou L, Zhang Y, Wu L, Xu H, Zhu G, Jang KS, Spencer RGM, Jeppesen E, et al (2022) Urban and agricultural land use regulates the molecular composition and bio-lability of fluvial dissolved organic matter in human-impacted southeastern China. Carbon Res 1(1). https://doi.org/10.1007/s44246-022-00020-6
Jia J, Dungait JA, Lu Y, Cui T, Yu G, Gao Y (2023) Inland water metabolic carbon processes and associated biological mechanisms that drive carbon source-sink instability. Innovation Geosci 1(3):100035
Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, Kirchman DL, Weinbauer MG, Luo T, Chen F et al (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8(8):593–599. https://doi.org/10.1038/nrmicro2386
Kida M, Kojima T, Tanabe Y, Hayashi K, Kudoh S, Maie N, Fujitake N (2019) Origin, distributions, and environmental significance of ubiquitous humic-like fluorophores in Antarctic lakes and streams. Water Res 163:114901. https://doi.org/10.1016/j.watres.2019.114901
Li Y, Zhou Y, Zhou L, Zhang Y, Xu H, Jang KS, Kothawala DN, Spencer RGM, Jeppesen E, Brookes JD et al (2022) Changes in water chemistry associated with rainstorm events increase carbon emissions from the inflowing river mouth of a major drinking water reservoir. Environ Sci Technol 56(22):16494–16505. https://doi.org/10.1021/acs.est.2c06405
Lu Y, Bauer JE, Canuel EA, Yamashita Y, Chambers RM, Jaffé R (2013) Photochemical and microbial alteration of dissolved organic matter in temperate headwater streams associated with different land use. J Geophys Res Biogeosci 118(2):566–580. https://doi.org/10.1002/jgrg.20048
McDonough LK, Andersen MS, Behnke MI, Rutlidge H, Oudone P, Meredith K, O’Carroll DM, Santos IR, Marjo CE, Spencer RGM et al (2022) A new conceptual framework for the transformation of groundwater dissolved organic matter. Nat Commun 13(1):2153. https://doi.org/10.1038/s41467-022-29711-9
McLaughlin C, Kaplan LA (2013) Biological lability of dissolved organic carbon in stream water and contributing terrestrial sources. Freshwater Sci 32(4):1219–1230
Salcher MM, Posch T, Pernthaler J (2013) In situ substrate preferences of abundant bacterioplankton populations in a prealpine freshwater lake. ISME J 7(5):896–907
Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, Dillon P, Finlay K, Fortino K, Knoll LB (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54(6):2298–2314
Xenopoulos MA, Barnes RT, Boodoo KS, Butman D, Catalán N, D’Amario SC, Fasching C, Kothawala DN, Pisani O, Solomon CT et al (2021) How humans alter dissolved organic matter composition in freshwater: relevance for the Earth’s biogeochemistry. Biogeochemistry. https://doi.org/10.1007/s10533-021-00753-3
Xia F, Liu Z, Zhao M, Li Q, Li D, Cao W, Zeng C, Hu Y, Chen B, Bao Q (2022) High stability of autochthonous dissolved organic matter in karst aquatic ecosystems: evidence from fluorescence. Water Res 220:118723
Zhang Y, van Dijk MA, Liu M, Zhu G, Qin B (2009) The contribution of phytoplankton degradation to chromophoric dissolved organic matter (CDOM) in eutrophic shallow lakes: field and experimental evidence. Water Res 43(18):4685–4697. https://doi.org/10.1016/j.watres.2009.07.024
Zhou Y, Liu M, Zhou L, Jang KS, Xu H, Shi K, Zhu G, Liu M, Deng J, Zhang Y et al (2020) Rainstorm events shift the molecular composition and export of dissolved organic matter in a large drinking water reservoir in China: high frequency buoys and field observations. Water Res 187:116471. https://doi.org/10.1016/j.watres.2020.116471
Zhou L, Zhou Y, Tang X, Zhang Y, Jang KS, Szekely AJ, Jeppesen E (2021) Resource aromaticity affects bacterial community successions in response to different sources of dissolved organic matter. Water Res 190:116776. https://doi.org/10.1016/j.watres.2020.116776
Zhou Y, Hiller C, Andersson S, Jakobsson E, Zhou L, Hawkes JA, Kothawala DN, Tranvik LJ (2023) Selective exclusion of aromatic organic carbon during lake ice formation. Geophys Res Lett 50(4):e2022GL101414. https://doi.org/10.1029/2022gl101414
Acknowledgements
We thank Anne Mette Poulsen from Aarhus University for editorial assistance, and the editor-in-chief and three anonymous reviewers for their helpful comments.
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This work was supported by the National Natural Science Foundation of China grants 42322104, 41930760, and 42207447), the Youth Innovation Promotion Association, CAS (2021312), the Provincial Natural Science Foundation of Jiangsu (BK20220162 and BK20220041), and NIGLAS Foundation (E1SL002 and 2022NIGLAS-CJH04). Erik Jeppesen was supported by the TÜBITAK program BIDEB2232 (project 118C250).
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Yongqiang Zhou and Yunlin Zhang acquired funding. Erik Jeppesen conducted investigation. Yunlin Zhang and Erik Jeppesen supervised the study. Conceptualization was performed by Fan Xia and Yongqiang Zhou. Fan Xiao prepared visualization. The first draft of the manuscript was written by Fan Xiao, Yongqiang Zhou, and Lei Zhou. Yongqiang Zhou, Lei Zhou, Yunlin Zhang, and Erik Jeppesen reviewed and edited the manuscript.
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Xia, F., Zhou, Y., Zhou, L. et al. Recalcitrant dissolved organic matter in lakes: a critical but neglected carbon sink. Carbon Res. 3, 47 (2024). https://doi.org/10.1007/s44246-024-00133-0
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DOI: https://doi.org/10.1007/s44246-024-00133-0