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Temperature sensitivity of soil respiration rates enhanced by microbial community response

Abstract

Soils store about four times as much carbon as plant biomass1, and soil microbial respiration releases about 60 petagrams of carbon per year to the atmosphere as carbon dioxide2. Short-term experiments have shown that soil microbial respiration increases exponentially with temperature3. This information has been incorporated into soil carbon and Earth-system models, which suggest that warming-induced increases in carbon dioxide release from soils represent an important positive feedback loop that could influence twenty-first-century climate change4. The magnitude of this feedback remains uncertain, however, not least because the response of soil microbial communities to changing temperatures has the potential to either decrease5,6,7 or increase8,9 warming-induced carbon losses substantially. Here we collect soils from different ecosystems along a climate gradient from the Arctic to the Amazon and investigate how microbial community-level responses control the temperature sensitivity of soil respiration. We find that the microbial community-level response more often enhances than reduces the mid- to long-term (90 days) temperature sensitivity of respiration. Furthermore, the strongest enhancing responses were observed in soils with high carbon-to-nitrogen ratios and in soils from cold climatic regions. After 90 days, microbial community responses increased the temperature sensitivity of respiration in high-latitude soils by a factor of 1.4 compared to the instantaneous temperature response. This suggests that the substantial carbon stores in Arctic and boreal soils could be more vulnerable to climate warming than currently predicted.

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Figure 1: Soil was sampled from boreal and Arctic, temperate, Mediterranean and tropical climates.
Figure 2: The patterns of CO2 flux that would be observed in the case of no response, compensatory and enhancing community-level responses.
Figure 3: The impact of the microbial community responses on the response of soil respiration to changes in temperature.

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Acknowledgements

We thank the staff of the Forestry Commission at Alice Holt Forest , T. Taylor from RSPB Aylesbeare Common Reserve, J. Harris from Cranfield University, C. Moscatelli and S. Marinari from Tuscia University, J. A. Carreira de la Fuente from the University of Jaén, R. Giesler from Umeå University and E. Cosio from The Pontifical Catholic University of Peru for help with site selection and soil sampling. We thank N. England for technical assistance with constructing the incubation system, J. Zaragoza Castells for help with soil sampling, A. Elliot for conducting the particle size analyses, J. Grapes for help with carbon and nitrogen analysis and S. Rouillard, H. Jones and T. Kurtén for assistance with graphics. This work was carried out with Natural Environment Research Council (NERC) funding (grant number NE/H022333/1). K.K. was supported by an Academy of Finland post-doctoral research grant while finalizing this manuscript. P.M. was supported by ARC FT110100457 and NERC NE/G018278/1, and B.K.S by the Grain Research and Development Corporation and ARC DP130104841.

Author information

Authors and Affiliations

Authors

Contributions

K.K. conducted the CO2 measurements and statistical analyses. K.K. and M.D.A. conducted the chloroform-fumigation extraction and qPCR analyses, respectively, and led the data analysis and interpretation. I.P.H. (lead investigator), P.A.W., D.W.H., B.K.S. and J.I.P. designed the study. G.I.Å. and K.K. were responsible for the modelling presented in the methods. K.K., I.P.H., J.A.J.D., D.W.H., J.-A.S., P.A.W., M.-T.S., F.G., G.B., P.M., A.T.N. and N.S. were involved in planning site selection and soil sampling. All authors were involved in interpreting the results and contributed to writing the manuscript.

Corresponding author

Correspondence to Kristiina Karhu.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 The results of the Q model, presenting the patterns that would be observed if there were no compensatory or enhancing microbial community responses.

a, Absolute respiration rates in the three treatments (control, cooled and rewarmed) are plotted against time. b, Changes in C availability over time, indicating that rates of C loss are greater in the control soils. c, Respiration rates are plotted against C loss, resulting in the differences between rewarmed- and control-soil respiration rates being eliminated. d, Respiration rates are normalized to rates immediately after cooling, and cooled and control treatments now show an identical relationship between respiration rate and C loss.

Extended Data Figure 2 Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 1A, 1C, 1D and 1G, including the 84-day pre-incubation period.

RRCT was calculated as control (open circles) respiration rate divided by rewarmed (black uptriangles) respiration rate based on the CO2 fluxes presented in the left panels (mean and standard error, n = 5, technical replicates). In the right panels relative respiration rates normalized for the time of cooling are shown for the control (open circles) and cooled treatments (open uptriangles). The final cooled treatment measurements were compared to the control treatment regression line at a similar C loss to calculate RRMT (control/cooled). Error bars represent standard error.

Extended Data Figure 3 Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 1H, 2C, 2D and 2G, including the 84-day pre-incubation period.

As for Extended Data Fig. 2.

Extended Data Figure 4 Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 2H, 3A, 3C and 3D, including the 84-day pre-incubation period.

As for Extended Data Fig. 2.

Extended Data Figure 5 Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 3G, 3H, 4A and 4C, including the 84-day pre-incubation period.

As for Extended Data Fig. 2.

Extended Data Figure 6 Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 4D, 4G, 4H and 5E_1, including the 84-day pre-incubation period.

As for Extended Data Fig. 2.

Extended Data Figure 7 Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 5E_2 and 5E_3, including the 84-day pre-incubation period.

As for Extended Data Fig. 2.

Extended Data Figure 8 The mean ± 95% confidence intervals of mass-specific RRMT values, calculated per CFE biomass (a) and per qPCR biomass (b).

Overall values (that is, including all data) and values for the different soil groups, based on ecosystem type, management, climate and the various soil properties, are presented (n is given in parentheses; bars are cut if they extend beyond 2.0 or 0.5, numbers on broken lines represent the final x-axis value rounded to 1 decimal place). One evergreen broadleaved forest soil (5E_1) had a biomass too low to be measured using the CFE method. Therefore in a, we cannot present confidence intervals for evergreen broadleaf forests because there are now only two replicates. Similarly, only two soils remained in the 0–2% C group, so these were combined with the 2–4% C group (we show the average for soils with 0–4% C). Values >1 and <1 indicate enhancing and compensatory responses, respectively. The patterns are very similar to RRMT calculated per gram of soil C (Fig. 3a).

Extended Data Table 1 Sampling site and soil characteristics

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Karhu, K., Auffret, M., Dungait, J. et al. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513, 81–84 (2014). https://doi.org/10.1038/nature13604

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