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Seasonality of lake microbial denitrification and its sensitivity to climate warming


Abstract

Lakes are expected to experience longer summer stratification and shorter winter mixing due to climate-induced warming. These changes will impact biogeochemical cycles, but how shifts in mixing might influence lake nitrogen removal via denitrification remains unconstrained. Here we used 15N-tracer assays, molecular techniques and flux measurements to establish the seasonal dynamics of denitrification in a eutrophic lake in Switzerland. We find that denitrification was disproportionately active during the winter mixed regime, potentially driven by a previously unrecognized chitinolytic–denitrifying microbial consortium. Moreover, denitrification was strongly governed by the relative availabilities of particulate organic carbon and nitrate. Leveraging these insights enabled accurate simulation of denitrification in a lake model, revealing that a worst-case climate scenario may shorten the mixing period by ~27 days and reduce denitrification by 8–13%, increasing nitrogen export to downstream ecosystems. We conclude that lake microbial denitrification, and its associated denitrifying consortium, will be weakened by climate change.

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Fig. 1: Vertical distribution of potential nitrogen transformation processes in Baldeggersee (Lake Baldegg).
The alternative text for this image may have been generated using AI.
Fig. 2: Seasonal dynamics of Baldeggersee physics, chemistry and nitrogen removal, along with associated key microbial players.
The alternative text for this image may have been generated using AI.
Fig. 3: Putative microbial consortium driving denitrification in the mixed regime.
The alternative text for this image may have been generated using AI.
Fig. 4: Future RCP scenario modelling of Baldeggersee’s physics and nitrogen removal.
The alternative text for this image may have been generated using AI.

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Data availability

Rate measurement data are available via Zenodo at https://doi.org/10.5281/zenodo.15351261 (ref. 80). The recovered MAGs discussed in this study have been deposited in the NCBI database under accession code PRJNA1259374, while the original metagenomic data are available under PRJNA726540 (ref. 31). Parameters used to calibrate the GLM used in this study are provided in Supplementary Tables 5–7. Source data are provided with this paper.

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Acknowledgements

We thank P. Kathriner, K. Beck and S. Robert for technical support, as well as B. Müller and K. Baumann for valuable scientific discussions. We are also grateful to R. Lovas and the Swiss cantonal authorities for providing access to Baldeggersee and water column chemistry data. We thank D. Bouffard and F. Bärenbold for providing meteorological forcing data and for discussions related to the initial model setup. This project was funded by the Swiss National Science Foundation through grants 188728 (awarded to M.F.L.) and 169142 (awarded to H.B.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the paper.

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Authors

Contributions

C.M.C., C.J.S. and M.F.L. designed the study. C.M.C., A.M., T.J.P. and C.F. completed the field sampling. C.M.C., A.M., T.J.P. and C.F. performed experiments. C.M.C., A.M., T.J.P. and C.F. analysed data. C.M.C. and H.B. analysed metagenomic data. C.M.C. calibrated and initialized the model and developed the conceptual framework for the paper. C.M.C. wrote the paper with substantial input from all co-authors.

Corresponding author

Correspondence to
Cameron M. Callbeck.

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Extended data

Extended Data Fig. 1 Chemical depth profiles and sediment-dwelling macrofauna in Baldeggersee.

(a,b,c) Example plots of oxygen, nitrate/ammonium, and sulfate/sulfide concentration profiles are shown. (a) In situ oxygen profile from a recovered sediment core is shown alongside a profile from a core subsequently spiked with additional macrofauna, demonstrating their potential to transport oxygen to deeper layers of the sediment. (d) Tubifex worms (top right panel) create dense burrow networks spanning from the superficial sediment layer down to 10 cm. In Baldeggersee, Tubifex worms occur at a faunal density of 8,500 individuals per m2. The nitrate anomalies (in panel b) and sulfide concentrations near the detection limit (in panel c) from 2–6 cm indicate active bio-irrigation. Bio-irrigation is likely also responsible for the elevated sulfide concentrations in the top centimeters of the sediment core, where reduced materials are excreted by Tubifex worms.

Source data

Extended Data Fig. 2 Water column rates of ammonium consumption associated with nitrification/assimilation processes in Baldeggersee.

The consumption of 15NH4+ (in 15NH4+ additions) over time was used to determine nitrification/assimilation rates. (a) Vertical distribution of nitrification/assimilation rates. Data are presented as mean values +/− standard deviation (n = 5; representing seasonal monthly data). (b) Rates of nitrification/assimilation under contrasting hydrodynamic regimes. The mixed regime is defined by a ≤ 1 °C difference between the surface and bottom waters (see Methods). Values are grouped by pooling all depth measurements within each mixing regime. The lower and upper hinges of the boxplots represent the 25th and 75th percentiles, and the solid lines indicate medians. Whiskers extend to the most extreme values within 1.5 × the interquartile range, and points beyond the whiskers represent outliers. (c) Seasonal trends for nitrification/assimilation activity based on observations (bars; mean ± standard error, n = 7; replicates represent multiple depths). Modeled nitrification data (red line) is also shown. See Supplementary Table 1 for details on stations and sample collection dates.

Source data

Extended Data Fig. 3 Relationship between RDNRA:Den and RPOC:NO3 in Lakes Baldeggersee (eutrophic) and Sarnersee (oligotrophic).

(a, b) Whisker plots comparing RDNRA:Den and RPOC:NO3 between Baldeggersee and Sarnersee. For RDNRA:Den, the sample size for both lakes is n = 5 (representing seasonal monthly data). For RPOC:NO3, the sample size is n = 8 for Baldeggersee and n = 7 for Sarnersee (representing seasonal monthly data). A Mann-Whitney test (one-tailed) was applied to evaluate the degree of variance between Lakes Baldeggersee and Sarnersee, with the asterisk(s) denoting the significance: *, p < 0.05; **, p < 0.01; ***, p « 0.01. For RDNRA:Den, the comparison between Baldeggersee and Sarnersee yielded p = 0.16, whereas for RPOC:NO3, the comparison yielded p = 0.01. The lower and upper hinges of the boxplots represent the 25th and 75th percentiles, crossed symbols denote means, and solid lines indicate medians. Whiskers extend from the median to 1.5 × the interquartile range, and data points beyond the whiskers represent outliers. (c) Correlation plot showing the observed relationship between RDNRA:Den and RPOC:NO3 for Baldeggersee (triangles) and Sarnersee (circles), based on monthly seasonal datasets from both lakes. Here, total POC flux is used (refocused plus euphotic-zone-derived components; Extended Data Fig. 4). A linear regression and t-test (two-tailed) were performed to assess the statistical significance (df = 7; p = 9.87 × 10−3, p < 0.01). Abbreviations: DNRA, dissimilatory nitrate reduction to ammonium; POC, particulate organic matter.

Source data

Extended Data Fig. 4 Observations of sediment refocusing and its coupling to wind-driven meteorological data in Baldeggersee.

Panels (a, b) show seasonal variability in water-column POC flux derived from upper and lower sediment traps previously reported by Müller et al.19. (a) The upper trap was positioned 15 m below the surface and reflects euphotic-zone-derived POC export, whereas the lower trap, located 3 m above the sediment, represents total POC flux (refocused/lateral plus vertical export). Data represent mean values of aggregated bi-weekly sediment trap measurements collected between 2017 and 2018 (mean ± SD; Mar–Sep n = 4, Oct n = 3, Nov n = 2). (b) Refocused POC flux was calculated as the difference between lower and upper trap fluxes. Wind-driven near-bed orbital velocities derived from meteorological forcing, which are the same data used to force the GLM-AED model, are also shown (mean ± SD; n = 30, representing daily values aggregated into monthly means for 2017–2022). Seasonal changes in particulate organic matter C:N ratios are additionally shown, with the Redfield ratio (C:N = 6.6) indicated for reference. (c) Boxplot comparing refocused POC fluxes between stratified and mixed regimes. The mixed regime is defined as a temperature difference of ≤ 1 °C between surface and bottom waters (see Methods). Weekly measurements were aggregated by mixing regime (stratified or mixed). Sample sizes were: orbital velocity, stratified/mixed n = 34/18; refocused POC, stratified/mixed n = 29/9. The lower and upper hinges represent the 25th and 75th percentiles, solid lines denote means, and dotted lines indicate medians. Whiskers extend to the most extreme values within 1.5 × the interquartile range. Statistical differences between regimes were assessed using a two-tailed Mann–Whitney test. Significance levels are indicated as *p < 0.05, **p < 0.01, and ***p < 0.001 (refocused POC: p = 0.0097; orbital velocity: p = 1.9 × 10−5). (d, f) Correlation analyses between observed biogeochemical and physical parameters (monthly data shown); Pearson correlation coefficients (two-tailed) and p-values are reported (C:N ratio vs refocused POC: df = 10, p = 0.0002; orbital velocity vs refocused POC: df = 10, p = 0.008; refocused POC vs nitrate flux: df = 5, p = 0.735; upper-trap POC vs nitrate flux: df = 6, p = 0.0179). (e) Empirical calibration curve used in the model to relate refocused POC flux to wind-driven orbital velocities (based on meteorological data).

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Extended Data Fig. 5 Improvement in model–observation agreement following the transition from the base to the refocused model for Baldeggersee.

(a-d) Boxplots comparing the base model versus the refocused POC model and the observations for the respective stratified and mixed regimes. The mixed regime is defined by a temperature difference of ≤ 1 °C between surface and bottom waters (see Methods). Observational data, collected on a bi-monthly or bi-weekly basis during seasonal sampling campaigns, were aggregated according to mixing regime (stratified or mixed). Model outputs, originally produced at daily resolution, were first aggregated to monthly means and subsequently grouped by mixing regime. The lower and upper hinges of the boxplots represent the 25th and 75th percentiles, solid red lines denote means, and dotted lines indicate medians. Whiskers extend to the most extreme values within 1.5 × the interquartile range. Statistical differences between regimes were evaluated using a two-tailed Mann–Whitney test. Significance levels are indicated as *p < 0.05, **p < 0.01, and ***p < 0.001; non-significant differences are denoted as ‘ns’ (model base POC, panel a: p = 0.0043; model base RPOC:NO3, panel b: p = 3.11 × 10−3; model base, model refocused, and observed denitrification, panel c: p = 3.11 × 10−3, 0.030, 0.013; model base DNRA, panel d: p = 1.56 × 10−3). Mixed-regime observations with limited sample size (n ≤ 10) include POC (n = 7), and RPOC:NO3 (n = 1); all other parameters have n > 10. (e) Seasonal variability of sediment denitrification and DNRA activity. (f) Comparison of the base and refocused POC model configurations in projections of Baldeggersee’s future capacity to remove fixed nitrogen. Data are presented as mean values +/− SEM (n = 29; replicates represent aggregated annual simulations).

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Extended Data Fig. 6 Organic matter composition and its turnover in Baldeggersee.

(a, b) Elemental C:N ratios of the settled particulate organic matter (POC). (a) The sample size for the mixed and stratified periods is n = 9 and n = 13 (representing seasonal monthly data), respectively. The lower and upper hinges of the boxplots represent the 25th and 75th percentiles, crossed symbols denote means, and solid lines indicate medians. Whiskers extend to the most extreme values within 1.5 × the interquartile range, and points beyond the whiskers represent outliers. (b) Shows the change in the C:N ratios of collected sediment trap material during the mixed (triangle) and stratified (square) periods, respectively. The water column sediment trap was positioned at the deepest point in the lake (red star in Fig. 1a) at 3 meters above the sediment. Note that in the mixed regime, the material collected in the trap is likely derived from sediment resuspension, providing useful insight into the changing composition of surface sediments deposited over this period. The Redfield C:N stoichiometry of 6.6 to 1 (grey dotted line) is used as a reference to indicate the reactivity of organic matter in Baldeggersee. During the winter mixed regime, which lasts 121 days in total, the C:N ratio surpasses the Redfield ratio at day 55. A linear regression is shown, and a two-tailed t-test was applied to determine statistical significance (mixed regime: df = 4, p = 5.31 × 10−3, p < 0.01; stratified regime: df = 8, p = 0.022, p < 0.05). (c) Seasonal rates of labile organic nitrogen remineralization to NH4+ (nmol cm−3 h−1) are shown for observations (bars; mean ± SEM, n = 10, aggregated sediment depth intervals), with modeled output overlaid (red line) to enable seasonal comparisons. We determined labile organic N remineralization rates by measuring the turnover of fresh 15N-labelled algal biomass (Spirulina platensi) in slurry addition experiments, specifically monitoring the production of 15NH4+. See Supplementary Table 1 for details on stations and sample collection dates.

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Extended Data Fig. 7 Vertical and temporal relationship between Bacteroidales (Bins 7, 8, 15, 18 M) and Methylophilales (Bin13M).

(a) Vertical abundances of Bacteroidales and Methylophilales were enumerated using CARD-FISH (see Methods). (b) Concentration profiles of monomers related to pectin (galacturonic acid m/z = 193) and chitin (glucosamine and N-acetyl-glucosamine m/z = 178 and 220, respectively). (c) Correlation between Bacteroidales (Bins 7, 8, 15, 18 M) and Methylophilales (Bin13M; Fig. 3b). Seasonal data refer to samples collected from 2017 to 2018 in Baldeggersee (Supplementary Table 1). Additionally, data from other lakes covering different trophic states are included in the correlation analysis, referred to as the ‘multi-lake study’. A linear regression is shown, and a two-tailed t-test was applied to assess statistical significance (df = 12; p = 4.30 × 10−6, p < 0.01).

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Extended Data Fig. 8 Future RCP scenario modeling of Baldeggersee biogeochemical fluxes.

(a, b, c, d) The baseline (outermost ring), RCP 2.6, RCP 4.5, and RCP 8.5 (innermost ring) scenarios are indicated. The black lines (across all panels) denote the beginning and end of the mixed regime (constrained by a temperature difference ≤1 °C between surface and bottom waters; see Methods). Regarding the inner bar plots, data are presented as mean values +/− SEM (n = 29; replicates represent aggregated annual simulations). The primary axis shows the total amount of the flux, scaled to Baldeggersee’s surface area (5.22 × 106 m2). A Welch test (one-tailed) was applied to evaluate the degree of variance between RCP 8.5 and the reference period, with the asterisk(s) denoting the significance: *, p < 0.05; **, p < 0.01; ***, p « 0.01, while non-significant differences are denoted ‘ns’ (NO3 flux: df = 55.1, p = 0.026, p < 0.05; O2 flux: df = 53.2, p = 5.54 × 10−11, p < 0.01). The secondary axis in the inner plots shows total fluxes partitioned between mixed and stratified conditions. Panel a presents the euphotic-zone-derived POC flux, whereas panel b shows total POC flux (refocused plus euphotic-zone-derived fluxes; see also Extended Data Fig. 5).

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Callbeck, C.M., Mazzoli, A., Paulus, T.J. et al. Seasonality of lake microbial denitrification and its sensitivity to climate warming.
Nat Microbiol (2026). https://doi.org/10.1038/s41564-026-02349-9

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