Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long-term warming.
carbon use efficiency
climate change
microbial temperature sensitivity
microbial thermal acclimation
soil carbon cycling
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
received:
12
08
2022
accepted:
18
11
2022
pubmed:
1
12
2022
medline:
16
2
2023
entrez:
30
11
2022
Statut:
ppublish
Résumé
Microbes are responsible for cycling carbon (C) through soils, and predicted changes in soil C stocks under climate change are highly sensitive to shifts in the mechanisms assumed to control the microbial physiological response to warming. Two mechanisms have been suggested to explain the long-term warming impact on microbial physiology: microbial thermal acclimation and changes in the quantity and quality of substrates available for microbial metabolism. Yet studies disentangling these two mechanisms are lacking. To resolve the drivers of changes in microbial physiology in response to long-term warming, we sampled soils from 13- and 28-year-old soil warming experiments in different seasons. We performed short-term laboratory incubations across a range of temperatures to measure the relationships between temperature sensitivity of physiology (growth, respiration, carbon use efficiency, and extracellular enzyme activity) and the chemical composition of soil organic matter. We observed apparent thermal acclimation of microbial respiration, but only in summer, when warming had exacerbated the seasonally-induced, already small dissolved organic matter pools. Irrespective of warming, greater quantity and quality of soil carbon increased the extracellular enzymatic pool and its temperature sensitivity. We propose that fresh litter input into the system seasonally cancels apparent thermal acclimation of C-cycling processes to decadal warming. Our findings reveal that long-term warming has indirectly affected microbial physiology via reduced C availability in this system, implying that earth system models including these negative feedbacks may be best suited to describe long-term warming effects on these soils.
Substances chimiques
Soil
0
Carbon
7440-44-0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1574-1590Subventions
Organisme : Joint Genome Institute
ID : 506489
Organisme : National Science Foundation
ID : DEB-1456528
Organisme : National Science Foundation
ID : DEB-1749206
Organisme : National Science Foundation
ID : DEB-1832210
Informations de copyright
© 2022 The Authors. Global Change Biology published by John Wiley & Sons Ltd.
Références
Abramoff, R. Z., & Finzi, A. C. (2015). Are above-and below-ground phenology in sync? New Phytologist, 205(3), 1054-1061.
Allison, S. D., Romero-Olivares, A. L., Lu, Y., Taylor, J. W., & Treseder, K. K. (2018). Temperature sensitivities of extracellular enzyme vmax and km across thermal environments. Global Change Biology, 24(7), 2884-2897.
Allison, S. D., Wallenstein, M. D., & Bradford, M. A. (2010). Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience, 3(5), 336-340.
Alster, C. J., Robinson, J. M., Arcus, V. L., & Schipper, L. A. (2022). Assessing thermal acclimation of soil microbial respiration using macromolecular rate theory. Biogeochemistry, 158, 1-11.
Berlemont, R., Martiny, A. C., & Kivisaar, M. (2015). Genomic potential for polysaccharide deconstruction in bacteria. Applied and Environmental Microbiology, 81(4), 1513-1519. https://doi.org/10.1128/AEM.03718-14
Bolan, N. S., Adriano, D. C., Kunhikrishnan, A., James, T., McDowell, R., & Senesi, N. (2011). Dissolved organic matter: Biogeochemistry, dynamics, and environmental significance in soils. Advances in Agronomy, 110, 1-75.
Bölscher, T., Ågren, G. I., & Herrmann, A. M. (2020). Land-use alters the temperature response of microbial carbon-use efficiency in soils-A consumption-based approach. Soil Biology and Biochemistry, 140, 107639. https://doi.org/10.1016/j.soilbio.2019.107639
Bradford, M. A. (2013). Thermal adaptation of decomposer communities in warming soils. Frontiers in Microbiology, 4, 333.
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 Letters, 11(12), 1316-1327.
Burns, R. G., & Dick, R. P. (Eds.). (2002). Enzymes in the environment: Activity, ecology, and applications. CRC Press.
Carey, J. C., Tang, J., Templer, P. H., Kroeger, K. D., Crowther, T. W., Burton, A. J., Dukes, J. S., Emmett, B., Frey, S. D., Heskel, M. A., Jiang, L., Machmuller, M. B., Mohan, J., Panetta, A. M., Reich, P. B., Reinsch, S., Wang, X., Allison, S. D., Bamminger, C., … Tietema, A. (2016). Temperature response of soil respiration largely unaltered with experimental warming. Proceedings of the National Academy of Sciences of the USA, 113(48), 13797-13802.
Cavicchioli, R., Ripple, W. J., Timmis, K. N., Azam, F., Bakken, L. R., Baylis, M., Behrenfeld, M. J., Boetius, A., Boyd, P. W., Classen, A. T., Crowther, T. W., Danovaro, R., Foreman, C. M., Huisman, J., Hutchins, D. A., Jansson, J. K., Karl, D. M., Koskella, B., Mark Welch, D. B., … Webster, N. S. (2019). Scientists' warning to humanity: Microorganisms and climate change. Nature Reviews Microbiology, 17, 569-586. https://doi.org/10.1038/s41579-019-0222-5
Cheeke, T. E., Phillips, R. P., Kuhn, A., Rösling, A., & Fransson, P. (2021). Variation in hyphal production rather than turnover regulates standing fungal biomass in temperate hardwood forests. Ecology, 102(3), e03260.
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Lawrence Erlbaum Associates. https://doi.org/10.4324/9780203771587
Contosta, A. R., Frey, S. D., & Cooper, A. B. (2011). Seasonal dynamics of soil respiration and n mineralization in chronically warmed and fertilized soils. Ecosphere, 2(3), 1-21.
Davidson, E. A., & Janssens, I. A. (2006). Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature, 440(7081), 165-173. https://doi.org/10.1038/nature04514
DeAngelis, K. M., Pold, G., Topçuoğlu, B. D., van Diepen, L. T. A., Varney, R. M., Blanchard, J. L., & Frey, S. D. (2015). Long-term forest soil warming alters microbial communities in temperate forest soils. Frontiers in Microbiology, 6, 104.
Domeignoz-Horta, L. A., Pold, G., Liu, X. J. A., Frey, S. D., Melillo, J. M., & DeAngelis, K. M. (2020). Microbial diversity drives carbon use efficiency in a model soil. Nature Communications, 11(1), 1-10. https://doi.org/10.1038/s41467-020-17502-z
Domeignoz-Horta, L. A., Shinfuku, M., Junier, P., Poirier, S., Verrecchia, E., Sebag, D., & DeAngelis, K. M. (2021). Direct evidence for the role of microbial community composition in the formation of soil organic matter composition and persistence. ISME Communications, 1(1), 64. https://doi.org/10.1038/s43705-021-00071-7
Feng, X., Simpson, A. J., Wilson, K. P., Williams, D. D., & Simpson, M. J. (2008). Increased cuticular carbon sequestration and lignin oxidation in response to soil warming. Nature Geoscience, 1(12), 836-839.
Fierer, N., Colman, B. P., Schimel, J. P., & Jackson, R. B. (2006). Predicting the temperature dependence of microbial respiration in soil: A continental-scale analysis. Global Biogeochemical Cycles, 20(3), GB3026. https://doi.org/10.1029/2005GB002644
Fierer, N., Jackson, J. A., Vilgalys, R., & Jackson, R. B. (2005). Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied Environmental Microbiology, 71(7), 4117-4120.
Frey, S., Drijber, R., Smith, H., & Melillo, J. (2008). Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biology and Biochemistry, 40(11), 2904-2907.
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 Change, 3(4), 395-398.
German, D. P., Weintraub, M. N., Grandy, A. S., Lauber, C. L., Rinkes, Z. L., & Allison, S. D. (2011). Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biology and Biochemistry, 43(7), 1387-1397.
Gommers, P., Van Schie, B., Van Dijken, J., & Kuenen, J. (1988). Biochemical limits to microbial growth yields: An analysis of mixed substrate utilization. Biotechnology and Bioengineering, 32(1), 86-94.
Gunina, A., & Kuzyakov, Y. (2022). From energy to (soil organic) matter. Global Change Biology, 28(7), 2169-2182. https://doi.org/10.1111/gcb.16071
Hall, E. K., Singer, G. A., Kainz, M. J., & Lennon, J. T. (2010). Evidence for a temperature acclimation mechanism in bacteria: An empirical test of a membrane-mediated trade-off. Functional Ecology, 24(4), 898-908.
Hartley, I. P., Heinemeyer, A., & Ineson, P. (2007). Effects of three years of soil warming and shading on the rate of soil respiration: Substrate availability and not thermal acclimation mediates observed response. Global Change Biology, 13(8), 1761-1770.
Huntemann, M., Ivanova, N., Mavromatis, K., Tripp, H., Paez-Espino, D., Tennessen, K., Palaniappan, K., Szeto, E., Pillay, M., Chen, I. A., Pati, A., Nielsen, T., Markowitz, V. M., & Kyrpides, N. C. (2016). The standard operating procedure of the DOE-JGI metagenome annotation pipeline (map v. 4). Standards in Genomic Sciences, 11, 88.
Kahm, M., Hasenbrink, G., Lichtenberg-Frat'e, H., Ludwig, J., & Kschischo, M. (2010). Grofit: Fitting biological growth curves with R. Journal of Statistical Software, 33(7), 1-21.
Kaiser, C., Koranda, M., Kitzler, B., Fuchslueger, L., Schnecker, J., Schweiger, P., Rasche, F., Zechmeister-Boltenstern, S., Sessitsch, A., & Richter, A. (2010). Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytologist, 187(3), 843-858.
Kirschbaum, M. U. (2004). Soil respiration under prolonged soil warming: Are rate reductions caused by acclimation or substrate loss? Global Change Biology, 10(11), 1870-1877. https://doi.org/10.1111/j.1365-2486.2004.00852.x
LaRowe, D. E., & Van Cappellen, P. (2011). Degradation of natural organic matter: A thermodynamic analysis. Geochimica et Cosmochimica Acta, 75(8), 2030-2042.
Lefcheck, J. S. (2016). Piecewisesem: Piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods in Ecology and Evolution, 7(5), 573-579. https://doi.org/10.1111/2041-210X.12512
Liu, X. J. A., Pold, G., Domeignoz-Horta, L. A., Geyer, K. M., Caris, H., Nicolson, H., Kemner, K. M., Frey, S. D., Jerry, M. M., & DeAngelis, K. M. (2021). Soil aggregate-mediated microbial responses to long-term warming. Soil Biology and Biochemistry, 152, 108055.
Lloyd, J., & Taylor, J. A. (1994). On the temperature dependence of soil respiration. Functional Ecology, 8(3), 315-323.
Luo, Y., Wan, S., Hui, D., & Wallace, L. L. (2001). Acclimatization of soil respiration to warming in a tall grass prairie. Nature, 413(6856), 622-625. https://doi.org/10.1038/35098065
Malik, A. A., Puissant, J., Goodall, T., Allison, S. D., & Griffiths, R. I. (2019). Soil microbial communities with greater investment in resource acquisition have lower growth yield. Soil Biology and Biochemistry, 132, 36-39. https://doi.org/10.1016/j.soilbio.2019.01.025
Malik, A., & Gleixner, G. (2013). Importance of microbial soil organic matter processing in dissolved organic carbon production. FEMS Microbiology Ecology, 86(1), 139-148.
McDonald, M. J. (2019). Microbial experimental evolution-A proving ground for evolutionary theory and a tool for discovery. EMBO Reports, 20(8), 1-14. https://doi.org/10.15252/embr.201846992
Melillo, J., Steudler, P., Aber, J., Newkirk, K., Lux, H., Bowles, F., Catricala, C., Magill, A., Ahrens, T., & Morrisseau, S. (2002). Soil warming and carbon-cycle feedbacks to the climate system. Science, 298(5601), 2173-2176.
Melillo, J. M., Frey, S. D., DeAngelis, K. M., Werner, W. J., Bernard, M. J., Bowles, F. P., Pold, G., Knorr, M. A., & Grandy, A. S. (2017). Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science, 358(6359), 101-105. https://doi.org/10.1126/science.aan2874
Mendiburu, F. D. (2019). Agricolae: Statistical procedures for agricultural research [Computer software manual]. (R package version 1.3-1).
Moinet, G. Y., Dhami, M. K., Hunt, J. E., Podolyan, A., Liáng, L. L., Schipper, L. A., Whitehead, D., Nuñez, J., Nascente, A., & Millard, P. (2021). Soil microbial sensitivity to temperature remains unchanged despite community compositional shifts along geothermal gradients. Global Change Biology, 27(23), 6217-6231. https://doi.org/10.1111/gcb.15878
Munger, W., & Wofsy, S. (2021). Biomass inventories at Harvard forest EMS tower since 1993. Harvard Forest Data Archive, 37, HF069. https://doi.org/10.6073/pasta/cd913a57d7f138b832b7f90b53ae21be
Muth, C. C., & Bazzaz, F. (2002). Tree canopy displacement at forest gap edges. Canadian Journal of Forest Research, 32(2), 247-254.
Nyamundanda, G., Brennan, L., & Gormley, I. C. (2010). Probabilistic principal component analysis for metabolomic data. BMC Bioinformatics, 11(1), 1-11.
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E., & Wagner, H. (2019). vegan: Community ecology package [Computer software manual]. (R package version 2.5-4).
Paradis, E., & Schliep, K. (2019). Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35(3), 526-528.
Pec, G. J., van Diepen, L. T. A., Knorr, M., Grandy, A. S., Melillo, J. M., DeAngelis, K. M., Blanchard, J. L., & Frey, S. D. (2021). Fungal community response to long-term soil warming with potential implications for soil carbon dynamics. Ecosphere, 12(5), e03460.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2019). nlme: Linear and nonlinear mixed effects models [Computer software manual]. (R package version 3.1-140).
Pisani, O., Frey, S. D., Simpson, A. J., & Simpson, M. J. (2015). Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level. Biogeochemistry, 123(3), 391-409.
Pold, G., Billings, A. F., Blanchard, J. L., Burkhardt, D. B., Frey, S. D., Melillo, J. M., Schnabel, J., van Diepen, L. T. A., & DeAngelis, K. (2016). Long-term warming alters carbohydrate degradation potential in temperate forest soils. ASM Journals on CD, 82(22), 6518-6530.
Pold, G., Domeignoz-Horta, L. A., & DeAngelis, K. M. (2020). Heavy and wet: The consequences of violating assumptions of measuring soil microbial growth efficiency using the 18O water method. Elementa: Science of the Anthropocene, 8(1), 069. https://doi.org/10.1525/elementa.069
Pold, G., Domeignoz-Horta, L. A., Morrison, E. W., Frey, S. D., Sistla, S. A., & DeAngelis, K. M. (2020). Carbon use efficiency and its temperature sensitivity Covary in soil bacteria. mBio, 11(1), e02293-19. https://doi.org/10.1128/mBio.02293-19
Pold, G., Grandy, A. S., Melillo, J. M., & DeAngelis, K. M. (2017). Changes in substrate availability drive carbon cycle response to chronic warming. Soil Biology and Biochemistry, 110, 68-78.
Price, P. B., & Sowers, T. (2004). Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proceedings of the National Academy of Sciences, 101(13), 4631-4636.
Rasche, F., Knapp, D., Kaiser, C., Koranda, M., Kitzler, B., Zechmeister-Boltenstern, S., Richter, A., & Sessitsch, A. (2011). Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest. The ISME Journal, 5(3), 389-402. https://doi.org/10.1038/ismej.2010.138
Ratkowsky, D. A., Olley, J., McMeekin, T. A., & Ball, A. (1982). Relationship between temperature and growth rate of bacterial cultures. Journal of Bacteriology, 149(1), 1-5. doi:10.1128/jb.149.1.1-5.1982
Robinson, J. M., O'Neill, T. A., Ryburn, J., Liang, L. L., Arcus, V. L., & Schipper, L. A. (2017). Rapid laboratory measurement of the temperature dependence of soil respiration and application to changes in three diverse soils through the year. Biogeochemistry, 133(1), 101-112. https://doi.org/10.1007/s10533-017-0314-0
Rocca, J. D., Simonin, M., Blaszczak, J. R., Ernakovich, J. G., Gibbons, S. M., Midani, F. S., & Washburne, A. D. (2019). The microbiome stress project: Toward a global meta-analysis of environmental stressors and their effects on microbial communities. Frontiers in Microbiology, 10(9), 3272.
Romero-Olivares, A. L., Allison, S. D., & Treseder, K. K. (2017). Soil microbes and their response to experimental warming over time: A meta-analysis of field studies. Soil Biology and Biochemistry, 107, 32-40. https://doi.org/10.1016/j.soilbio.2016.12.026
Roy Chowdhury, P., Golas, S. M., Alteio, L. V., Stevens, J. T. E., Billings, A. F., Blanchard, J. L., Melillo, J. M., & DeAngelis, K. (2021). The transcriptional response of soil bacteria to long-term warming and short-term seasonal fluctuations in a terrestrial forest. Frontiers in Microbiology, 12, 666558. https://doi.org/10.3389/fmicb.2021.666558
Sanderman, J., & Grandy, A. S. (2020). Ramped thermal analysis for isolating biologically meaningful soil organic matter fractions with distinct residence times. The Soil, 6(1), 131-144.
Sarkar, D. (2008). Lattice: Multivariate data visualization with R. Springer.
Sebag, D., Verrecchia, E. P., Cecillon, L., Adatte, T., Albrecht, R., Aubert, M., Bureau, F., Cailleau, G., Copard, Y., Decaens, T., Disnar, J., Hetényi, M., Nyilas, T., & Trombino, T. (2016). Dynamics of soil organic matter based on new Rock-Eval indices. Geoderma, 284, 185-203. https://doi.org/10.1016/j.geoderma.2016.08.025
Simpson, G. L. (2022). permute: Functions for generating restricted permutations of data [Computer software manual]. (R package version 0.9-7).
Söllinger, A., Séneca, J., Dahl, M. B., Motleleng, L. L., Prommer, J., Verbruggen, E., Sigurdsson, B. D., Janssens, I., Peñuelas, J., Urich, T., Richter, A., & Tveit, A. T. (2022). Down-regulation of the bacterial protein biosynthesis machinery in response to weeks, years, and decades of soil warming. Science Advances, 8(12), eabm3230. https://doi.org/10.1126/sciadv.abm3230
Soucémarianadin, L., Cécillon, L., Chenu, C., Baudin, F., Nicolas, M., Girardin, C., & Barré, P. (2018). Is Rock-Eval 6 thermal analysis a good indicator of soil organic carbon lability? A method-comparison study in forest soils. Soil Biology and Biochemistry, 117, 108-116. doi:10.1016/j.soilbio.2017.10.025
Spohn, M., Klaus, K., Wanek, W., & Richter, A. (2016). Microbial carbon use efficiency and biomass turnover times depending on soil depth-implications for carbon cycling. Soil Biology and Biochemistry, 96, 74-81.
Sprouffske, K., & Wagner, A. (2016). Growthcurver: An R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinformatics, 17(1). https://doi.org/10.1186/s12859-016-1016-7
Torchiano, M. (2020). effsize: Efficient effect size computation [Computer software manual]. (R package version 0.8.1). https://doi.org/10.5281/zenodo.1480624
Van Gestel, N., Shi, Z., Van Groenigen, K. J., Osenberg, C. W., Andresen, L. C., Dukes, J. S., Hovenden, M. J., Luo, Y., Michelsen, A., Pendall, E., Reich, P. B., Schuur, E. A. G., & Hungate, B. A. (2018). Predicting soil carbon loss with warming. Nature, 554(7693), E4-E5. https://doi.org/10.1038/nature25745
VandenEnden, L., Anthony, M. A., Frey, S. D., & Simpson, M. J. (2021). Biogeochemical evolution of soil organic matter composition after a decade of warming and nitrogen addition. Biogeochemistry, 156(2), 161-175.
Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). Springer.
Walker, T. W., Janssens, I. A., Weedon, J. T., Sigurdsson, B. D., Richter, A., Peñuelas, J., Leblans, N. I. W., Bahn, M., Bartrons, M., de Jonge, C., Fuchslueger, L., Gargallo-Garriga, A., Gunnarsdóttir, G. E., Marañón-Jiménez, S., Oddsdóttir, E. S., Ostonen, I., Poeplau, C., Prommer, J., Radujković, D., … Verbruggen, E. (2020). A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem. Nature Ecology and Evolution, 4(1), 101-108. https://doi.org/10.1038/s41559-019-1055-3
Walker, T. W., Kaiser, C., Strasser, F., Herbold, C. W., Leblans, N. I., Woebken, D., Janssens, I. A., Sigurdsson, B. D., & Richter, A. (2018). Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nature Climate Change, 8(10), 885-889. https://doi.org/10.1038/s41558-018-0259-x
Wardle, D. A., Bardgett, R. D., Klironomos, J. N., Setälä, H., van der Putten, W. H., & Wall, D. H. (2004). Ecological linkages between aboveground and belowground biota. Science, 304(5677), 1629-1633. https://doi.org/10.1126/science.1094875
Wickham, H. (2007). Reshaping data with the reshape package. Journal of Statistical Software, 21(12), 1-20.
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer-Verlag.
Wickham, H., François, R., Henry, L., & Muller, K. (2022). dplyr: A grammar of data manipulation [computer software manual]. (R package version 1.0.8).
Yao, Y., Sun, T., Wang, T., Ruebel, O., Northen, T., & Bowen, B. P. (2015). Analysis of metabolomics datasets with high-performance computing and metabolite atlases. Metabolites, 5(3), 431-442.
Yarwood, S. A., Myrold, D. D., & Hogberg, M. N. (2009). Termination of belowground C allocation by trees alters soil fungal and bacterial communities in a boreal forest. FEMS Microbiology Ecology, 70(1), 151-162. https://doi.org/10.1111/j.1574-6941.2009.00733.x
Zhalnina, K., Louie, K. B., Hao, Z., Mansoori, N., da Rocha, U. N., Shi, S., Cho, H., Karaoz, U., Loqué, D., Bowen, B. P., Firestone, M. K., Northen, T. R., & Brodie, E. L. (2018). Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nature Microbiology, 3(4), 470-480. https://doi.org/10.1038/s41564-018-0129-3