Low soil moisture suppresses microbial thermal compensatory response under drought and rewetting

Abstract

Climate warming is exacerbating soil drought and precipitation events, as well as different land use types lead varying nutrient inputs, driving substantial shifts in microbial communities that may influence soil respiration. Microbial thermal compensation mechanisms serve as critical biological regulators, alleviating the warming-induced enhancement of soil respiration. However, the effects of soil moisture and land use types on the thermal responses of microbial respiration remain insufficiently understood and constrained. Here, we collected soil from four distinct sites, each comprising both farmland and forest, and conducted indoor experiments to simulate drought and rewetting events. We then assayed the thermal responses of microbial respiration rates at 40% and 60% of soil water holding capacity (WHC) in the first moisture incubation experiment, and at a consistent moisture level (60% WHC) in the subsequent recovery moisture experiment. Our results showed that low soil moisture suppressed the thermal compensatory response while enhancing respiration in both soil types after drought and rewetting. In the incubation experiment, the respiratory response of soil microbes to warming was stronger in farmland ecosystems than in forest ecosystems. Notably, farmland soils under prior low moisture stress exhibited a high thermal compensatory response of microbial respiration after rewetting–opposite to forest soils. Overall, our findings suggested that climate warming-induced drought might weaken the thermal compensatory response of microbial respiration in both farmland and forest soils, with this effect persisting after rewetting. By improving estimates of projected soil carbon losses to the atmosphere via respiration, our work contributes to more accurate predictive modelling of carbon dynamics in farmland and forest soils under climate warming.

Graphical abstract

Keywords

climate warming / microbial respiration / thermal response / soil moisture / land use types

Highlight

	● Warming boosted microbial respiration under drought (40% WHC).
	● Low moisture suppressed microbial thermal compensation under drought; this suppression weakened during recovery.
	● Farmland soils showed stronger warming-induced respiratory responses than forests.
	● Land use types significantly affected both MCC and MCR values.

References

[1] Atkin, O.K., Tjoelker, M.G., 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science8, 343–351.

[2] Attiwill, P.M., Adams, M.A., 1993. Nutrient cycling in forests. New Phytologist124, 561–582.

[3] Bardgett, R.D., Freeman, C., Ostle, N.J., 2008. Microbial contributions to climate change through carbon cycle feedbacks. The ISME Journal2, 805–814.

[4] Beugnon, R., Eisenhauer, N., Lochner, A., Blechinger, M.J., Buhr, P.E., Cesarz, S., Farfan, M.A., Ferlian, O., Rompeltien Howard, A.J., Huang, Y.Y., Kuhlmann, B.S., Lienicke, N., Mählmann, S., Nowka, A., Petereit, E., Ristok, C., Schädler, M., Schmid, J.T.M., Schulte, L.J., Seim, K.L., Thouvenot, L., Tremmel, R., Weber, L., Weitowitz, J., Yi, H.M., Sünnemann, M., 2025. Sustainable land use enhances soil microbial respiration responses to experimental heat stress. Global Change Biology31, e70214.

[5] Bradford, M.A., 2013. Thermal adaptation of decomposer communities in warming soils. Frontiers in Microbiology4, 333.

[6] Bradford, M.A., Davies, C.A., Frey, S.D., Maddox, T.R., Melillo, J.M., Mohan, J.E., Reynolds, J.F., Treseder, K.K., Wallenstein, M.D., 2008. Thermal adaptation of soil microbial respiration to elevated temperature. Ecology Letters11, 1316–1327.

[7] Bradford, M.A., McCulley, R.L., Crowther, T.W., Oldfield, E.E., Wood, S.A., Fierer, N., 2019. Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation. Nature Ecology & Evolution3, 223–231.

[8] Bradford, M.A., Watts, B.W., Davies, C.A., 2010. Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Global Change Biology16, 1576–1588.

[9] Bradford, M.A., Wieder, W.R., Bonan, G.B., Fierer, N., Raymond, P.A., Crowther, T.W., 2016. Managing uncertainty in soil carbon feedbacks to climate change. Nature Climate Change6, 751–758.

[10] Briones, M.J.I., McNamara, N.P., Poskitt, J., Crow, S.E., Ostle, N.J., 2014. Interactive biotic and abiotic regulators of soil carbon cycling: evidence from controlled climate experiments on peatland and boreal soils. Global Change Biology20, 2971–2982.

[11] Čapek, P., Starke, R., Hofmockel, K.S., Bond-Lamberty, B., Hess, N., 2019. Apparent temperature sensitivity of soil respiration can result from temperature driven changes in microbial biomass. Soil Biology and Biochemistry135, 286–293.

[12] Casals, P., Lopez-Sangil, L., Carrara, A., Gimeno, C., Nogués, S., 2011. Autotrophic and heterotrophic contributions to short-term soil CO₂ efflux following simulated summer precipitation pulses in a Mediterranean dehesa. Global Biogeochemical Cycles25, GB3012.

[13] Cohen, J., 1988. Statistical Power Analysis for the Behavioral Sciences. 2nd ed. Hillsdale: Lawrence Erlbaum Associates.

[14] Dacal, M., Bradford, M.A., Plaza, C., Maestre, F.T., García-Palacios, P., 2019. Soil microbial respiration adapts to ambient temperature in global drylands. Nature Ecology & Evolution3, 232–238.

[15] Dacal, M., García-Palacios, P., Asensio, S., Cano-Díaz, C., Gozalo, B., Ochoa, V., Maestre, F.T., 2020. Contrasting mechanisms underlie short- and longer-term soil respiration responses to experimental warming in a dryland ecosystem. Global Change Biology26, 5254–5266.

[16] de Nijs, E.A., Hicks, L.C., Leizeaga, A., Tietema, A., Rousk, J., 2019. Soil microbial moisture dependences and responses to drying–rewetting: the legacy of 18 years drought. Global Change Biology25, 1005–1015.

[17] Fierer, N., Lauber, C.L., Ramirez, K.S., Zaneveld, J., Bradford, M.A., Knight, R., 2012. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. The ISME Journal6, 1007–1017.

[18] Frey, S.D., Lee, J., Melillo, J.M., Six, J., 2013. The temperature response of soil microbial efficiency and its feedback to climate. Nature Climate Change3, 395–398.

[19] García-Palacios, P., Crowther, T.W., Dacal, M., Hartley, I.P., Reinsch, S., Rinnan, R., Rousk, J., van den Hoogen, J., Ye, J.S., Bradford, M.A., 2021. Evidence for large microbial-mediated losses of soil carbon under anthropogenic warming. Nature Reviews Earth & Environment2, 507–517.

[20] Hartley, I.P., Heinemeyer, A., Evans, S.P., Ineson, P., 2007. The effect of soil warming on bulk soil vs. rhizosphere respiration. Global Change Biology13, 2654–2667.

[21] Hawkes, C.V., Keitt, T.H., 2015. Resilience vs. historical contingency in microbial responses to environmental change. Ecology Letters18, 612–625.

[22] He, Y., Zhuang, Q., Harden, J.W., McGuire, A.D., Fan, Z., Liu, Y., Wickland, K.P., 2014. The implications of microbial and substrate limitation for the fates of carbon in different organic soil horizon types of boreal forest ecosystems: a mechanistically based model analysis. Biogeosciences11, 4477–4491.

[23] Hicks, L.C., Leizeaga, A., Paredes, C.C., Brangarí, A.C., Tájmel, D., Wondie, M., Sandén, H., Rousk, J., 2025. Simulated climate change enhances microbial drought resilience in Ethiopian croplands but not forests. Global Change Biology31, e70065.

[24] Hicks, L.C., Lin, S., Rousk, J., 2022. Microbial resilience to drying-rewetting is partly driven by selection for quick colonizers. Soil Biology and Biochemistry167, 108581.

[25] Hu, S.D., Li, Y.F., Chang, S.X., Li, Y.C., Yang, W.J., Fu, W.J., Liu, J., Jiang, P.K., Lin, Z.W. 2018. Soil autotrophic and heterotrophic respiration respond differently to land-use change and variations in environmental factors.. Agricultural and Forest Meteorology250–251, 290–298.

[26] IPCC, 2021. Climate Change 2021: the physical science basis. Working group I contribution to the 6th assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press.

[27] IPCC, 2023. Climate change 2023: synthesis report. Contribution of working groups I, II and III to the sixth assessment report of the intergovernmental panel on climate change. Geneva: IPCC, 35–115.

[28] Jakobsen, M.D., Sundstrup, E., Brandt, M., Jay, K., Aagaard, P., Andersen, L.L., 2015. Effect of workplace-versus home-based physical exercise on musculoskeletal pain among healthcare workers: a cluster randomized controlled trial. Scandinavian Journal of Work, Environment & Health41, 153–163.

[29] Leff, J.W., Jones, S.E., Prober, S.M., Barberán, A., Borer, E.T., Firn, J.L., Harpole, W.S., Hobbie, S.E., Hofmockel, K.S., Knops, J.M.H., McCulley, R.L., Pierre, K.L., Risch, A.C., Seabloom, E.W., Schütz, M., Steenbock, C., Stevens, C.J., Fierer, N., 2015. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proceedings of the National Academy of Sciences of the United States of America112, 10967–10972.

[30] Lehmann, J., Kleber, M., 2015. The contentious nature of soil organic matter. Nature528, 60–68.

[31] Leizeaga, A., Hicks, L.C., Manoharan, L., Hawkes, C.V., Rousk, J., 2021. Drought legacy affects microbial community trait distributions related to moisture along a savannah grassland precipitation gradient. Journal of Ecology109, 3195–3210.

[32] Lellei-Kovács, E., Botta-Dukát, Z., Ónodi, G., Mojzes, A., Kröel-Dulay, G., 2025. The negative legacy effect of extreme drought on soil respiration is unaffected by post-drought precipitation regime in a temperate grassland. Global Change Biology31, e70083.

[33] Li, J.T., Zhang, Y., Chen, H.Y., Sun, H.M., Tian, W.T., Li, J.Q., Liu, X., Zhou, S.R., Fang, C.M., Li, B., Nie, M., 2023a. Low soil moisture suppresses the thermal compensatory response of microbial respiration. Global Change Biology29, 874–889.

[34] Li, Q., Leroy, F., Zocatelli, R., Gogo, S., Jacotot, A., Guimbaud, C., Laggoun-Défarge, F., 2021. Abiotic and biotic drivers of microbial respiration in peat and its sensitivity to temperature change. Soil Biology and Biochemistry153, 108077.

[35] Li, X.K., Leizeaga, A., Rousk, J., Hugelius, G., Manzoni, S., 2023b. Drying intensity and acidity slow down microbial growth recovery after rewetting dry soils. Soil Biology and Biochemistry184, 109115.

[36] Li, X.K., Leizeaga, A., Rousk, J., Zhou, S.Y., Hugelius, G., Manzoni, S., 2024. Recovery of soil microbial metabolism after rewetting depends on interacting environmental conditions and changes in functional groups and life history strategies. Global Change Biology30, e17522.

[37] Liu, W.X., Zhang, Z., Wan, S.Q., 2009. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Global Change Biology15, 184–195.

[38] Manzoni, S., Schimel, J.P., Porporato, A., 2012. Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology93, 930–938.

[39] Melillo, J.M., Steudler, P.A., Aber, J.D., Newkirk, K., Lux, H., Bowles, F.P., Catricala, C., Magill, A., Ahrens, T., Morrisseau, S., 2002. Soil warming and carbon-cycle feedbacks to the climate system. Science298, 2173–2176.

[40] Moyano, F.E., Manzoni, S., Chenu, C., 2013. Responses of soil heterotrophic respiration to moisture availability: an exploration of processes and models. Soil Biology and Biochemistry59, 72–85.

[41] Nie, M., Pendall, E., Bell, C., Gasch, C.K., Raut, S., Tamang, S., Wallenstein, M.D., 2013. Positive climate feedbacks of soil microbial communities in a semi-arid grassland. Ecology Letters16, 234–241.

[42] Nottingham, A.T., Scott, J.J., Saltonstall, K., Broders, K., Montero-Sanchez, M., Püspök, J., Bååth, E., Meir, P., 2022. Microbial diversity declines in warmed tropical soil and respiration rise exceed predictions as communities adapt. Nature Microbiology7, 1650–1660.

[43] Qu, L.R., Wang, C., Manzoni, S., Dacal, M., Maestre, F.T., Bai, E., 2024. Stronger compensatory thermal adaptation of soil microbial respiration with higher substrate availability. The ISME Journal18, wrae025.

[44] Reinsch, T., Loges, R., Kluß, C., Taube, F., 2018. Effect of grassland ploughing and reseeding on CO₂ emissions and soil carbon stocks. Agriculture, Ecosystems & Environment265, 374–383.

[45] Roller, B.R.K., Schmidt, T.M., 2015. The physiology and ecological implications of efficient growth. The ISME Journal9, 1481–1487.

[46] Schädler, M., Buscot, F., Klotz, S., Reitz, T., Durka, W., Bumberger, J., Merbach, I., Michalski, S.G., Kirsch, K., Remmler, P., Schulz, E., Auge, H., 2019. Investigating the consequences of climate change under different land-use regimes: a novel experimental infrastructure. Ecosphere10, e02635.

[47] Schimel, J., Balser, T.C., Wallenstein, M., 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology88, 1386–1394.

[48] Schimel, J.P., 2018. Life in dry soils: effects of drought on soil microbial communities and processes. Annual Review of Ecology, Evolution, and Systematics49, 409–432.

[49] Schlaepfer, D.R., Bradford, J.B., Lauenroth, W.K., Munson, S.M., Tietjen, B., Hall, S.A., Wilson, S.D., Duniway, M.C., Jia, G.S., Pyke, D.A., Lkhagva, A., Jamiyansharav, K., 2017. Climate change reduces extent of temperate drylands and intensifies drought in deep soils. Nature Communications8, 14196.

[50] Seebacher, F., White, C.R., Franklin, C.E., 2015. Physiological plasticity increases resilience of ectothermic animals to climate change. Nature Climate Change5, 61–66.

[51] Shao, P., Zeng, X.B., Moore, D.J.P., Zeng, X.D., 2013. Soil microbial respiration from observations and Earth System Models. Environmental Research Letters8, 034034.

[52] Sinsabaugh, R.L., Follstad Shah, J.J., 2012. Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology, Evolution, and Systematics43, 313–343.

[53] Sun, W.H., Zhao, X.N., Ling, Q., Li, H.C., Gao, X.D., 2018. Revegetation modifies patterns of temporal soil respiration responses to extreme-drying-and-rewetting in a semiarid ecosystem. Plant and Soil433, 227–241.

[54] Tang, Y.Q., Winterfeldt, S., Brangarí, A.C., Hicks, L.C., Rousk, J., 2023. Higher resistance and resilience of bacterial growth to drought in grasslands with historically lower precipitation. Soil Biology and Biochemistry177, 108889.

[55] Veach, A.M., Zeglin, L.H., 2020. Historical drought affects microbial population dynamics and activity during soil drying and re-wet. Microbial Ecology79, 662–674.

[56] Wang, W.J., Dalal, R.C., Moody, P.W., Smith, C.J., 2003. Relationships of soil respiration to microbial biomass, substrate availability and clay content. Soil Biology and Biochemistry35, 273–284.

[57] Wang, Y.F., Hao, Y.B., Cui, X.Y., Zhao, H.T., Xu, C.Y., Zhou, X.Q., Xu, Z.H., 2014. Responses of soil respiration and its components to drought stress. Journal of Soils and Sediments14, 99–109.

[58] Ye, J.S., Bradford, M.A., Maestre, F.T., Li, F.M., García-Palacios, P., 2020. Compensatory thermal adaptation of soil microbial respiration rates in global croplands. Global Biogeochemical Cycles34, e2019GB006507.

[59] Zhang, Y.J., Guo, S.L., Liu, Q.F., Jiang, J.S., Wang, R., Li, N.N., 2015. Responses of soil respiration to land use conversions in degraded ecosystem of the semi-arid Loess Plateau. Ecological Engineering74, 196–205.

[60] Zheng, P.F., Wang, D.D., Yu, X.X., Jia, G.D., Liu, Z.Q., Wang, Y.S., Zhang, Y.E., 2021. Effects of drought and rainfall events on soil autotrophic respiration and heterotrophic respiration. Agriculture, Ecosystems & Environment308, 107267.

[61] Zheng, Q., Hu, Y.T., Zhang, S.S., Noll, L., Böckle, T., Richter, A., Wanek, W., 2019. Growth explains microbial carbon use efficiency across soils differing in land use and geology. Soil Biology and Biochemistry128, 45–55.

[62] Zhu, L.L., Bloomfield, K.J., Asao, S., Tjoelker, M.G., Egerton, J.J.G., Hayes, L., Weerasinghe, L.K., Creek, D., Griffin, K.L., Hurry, V., Liddell, M., Meir, P., Turnbull, M.H., Atkin, O.K., 2021. Acclimation of leaf respiration temperature responses across thermally contrasting biomes. New Phytologist229, 1312–1325.

RIGHTS & PERMISSIONS

Higher Education Press