in

Microbial diversity declines in warmed tropical soil and respiration rise exceed predictions as communities adapt

  • Cavicchioli, R. et al. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Jackson, R. B. et al. The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu. Rev. Ecol. Evol. Syst. 48, 419–445 (2017).

    Article 

    Google Scholar 

  • Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • IPCC. Climate Change 2021: The Physical Science Basis. (eds Masson-Delmotte, V. et al.) (Cambridge Univ. Press, in press).

  • Mora, C. et al. The projected timing of climate departure from recent variability. Nature 502, 183–187 (2013).

  • Wood, T. E. et al. in Ecosystem Consequences of Soil Warming: Microbes, Vegetation, Fauna and Soil Biogeochemistry (ed. Mohan, J.) Ch. 14 (Academic Press, 2019).

  • Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • van Gestel, N. et al. Predicting soil carbon loss with warming. Nature 554, E4–E5 (2018).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Melillo, J. M. et al. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358, 101–104 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Romero-Olivares, A. L., Allison, S. D. & Treseder, K. K. Soil microbes and their response to experimental warming over time: a meta-analysis of field studies. Soil Biol. Biochem. 107, 32–40 (2017).

    CAS 
    Article 

    Google Scholar 

  • Anderson-Teixeira, K. J., Wang, M. M. H., McGarvey, J. C. & LeBauer, D. S. Carbon dynamics of mature and regrowth tropical forests derived from a pantropical database (TropForC-db). Glob. Change Biol. 22, 1690–1709 (2016).

    Article 

    Google Scholar 

  • Nottingham, A. T., Meir, P., Velasquez, E. & Turner, B. L. Soil carbon loss by experimental warming in a tropical forest. Nature 584, 234–237 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kimball, B. A. et al. Infrared heater system for warming tropical forest understory plants and soils. Ecol. Evol. 8, 1932–1944 (2018).

  • DeAngelis, K. M. et al. Long-term forest soil warming alters microbial communities in temperate forest soils. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.00104 (2015)

  • Bååth, E. Temperature sensitivity of soil microbial activity modeled by the square root equation as a unifying model to differentiate between direct temperature effects and microbial community adaptation. Glob. Change Biol. 24, 2850–2861 (2018).

    Article 

    Google Scholar 

  • Wieder, W. R., Bonan, G. B. & Allison, S. D. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Change 3, 909–912 (2013).

    CAS 
    Article 

    Google Scholar 

  • Ratkowsky, D. A., Olley, J., Mcmeekin, T. A. & Ball, A. Relationship between temperature and growth-rate of bacterial cultures. J. Bacteriol. 149, 1–5 (1982).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Rinnan, R., Rousk, J., Yergeau, E., Kowalchuk, G. A. & Bååth, E. Temperature adaptation of soil bacterial communities along an Antarctic climate gradient: predicting responses to climate warming. Glob. Change Biol. 15, 2615–2625 (2009).

    Article 

    Google Scholar 

  • Nottingham, A. T., Bååth, E., Reischke, S., Salinas, N. & Meir, P. Adaptation of soil microbial growth to temperature: using a tropical elevation gradient to predict future changes. Glob. Change Biol. https://doi.org/10.1111/gcb.14502 (2019).

  • Li, J. Q., Bååth, E., Pei, J. M., Fang, C. M. & Nie, M. Temperature adaptation of soil microbial respiration in alpine, boreal and tropical soils: an application of the square root (Ratkowsky) model. Glob. Change Biol. 27, 1281–1292 (2021).

    CAS 
    Article 

    Google Scholar 

  • Rousk, J., Frey, S. D. & Bååth, E. Temperature adaptation of bacterial communities in experimentally warmed forest soils. Glob. Change Biol. 18, 3252–3258 (2012).

    Article 

    Google Scholar 

  • Nottingham, A. T. et al. Annual to decadal temperature adaptation of the soil bacterial community after translocation across an elevation gradient in the Andes. Soil Biol. Biochem. 158, 108217 (2021).

    CAS 
    Article 

    Google Scholar 

  • Nottingham, A. T. et al. Microbial responses to warming enhance soil carbon loss following translocation across a tropical forest elevation gradient. Ecol. Lett. 22, 1889–1899 (2019).

    PubMed 
    Article 

    Google Scholar 

  • Donhauser, J., Niklaus, P. A., Rousk, J., Larose, C. & Frey, B. Temperatures beyond the community optimum promote the dominance of heat-adapted, fast growing and stress resistant bacteria in alpine soils. Soil Biol. Biochem. 148, 107873 (2020).

    CAS 
    Article 

    Google Scholar 

  • Mangan, S. A. et al. Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466, 752–755 (2010).

  • Pold, G., Melillo, J. M. & DeAngelis, K. M. Two decades of warming increases diversity of a potentially lignolytic bacterial community. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.00480 (2015).

  • Zhou, J. Z. et al. Temperature mediates continental-scale diversity of microbes in forest soils. Nat. Commun. 7, 12083 (2016).

  • Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1256688 (2014).

  • Wu, L. et al. Reduction of microbial diversity in grassland soil is driven by long-term climate warming. Nat. Microbiol. 7, 1054–1062 (2022).

  • Oliverio, A. M., Bradford, M. A. & Fierer, N. Identifying the microbial taxa that consistently respond to soil warming across time and space. Glob. Change Biol. 23, 2117–2129 (2017).

    Article 

    Google Scholar 

  • Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Spracklen, D. V., Baker, J. C. A., Garcia-Carreras, L. & Marsham, J. H. The effects of tropical vegetation on rainfall. Annu. Rev. Env. Resour. 43, 193–218 (2018).

    Article 

    Google Scholar 

  • Bradford, M. A. Thermal adaptation of decomposer communities in warming soils. Front. Microbiol. https://doi.org/10.3389/Fmicb.2013.00333 (2013).

  • Pietikäinen, J., Pettersson, M. & Bååth, E. Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol. Ecol. 52, 49–58 (2005).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Mori, A. S. et al. Biodiversity–productivity relationships are key to nature-based climate solutions. Nat. Clim. Change 11, 543–550 (2021).

    Article 

    Google Scholar 

  • Delgado-Baquerizo, M. et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat. Ecol. Evol. 4, 210–220 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Wagg, C., Bender, S. F., Widmer, F. & van der Heijden, M. G. A. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl Acad. Sci. USA 111, 5266–5270 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Nottingham, A. T. et al. Microbes follow Humboldt: temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes. Ecology 99, 2455–2466 (2018).

    PubMed 
    Article 

    Google Scholar 

  • Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article 

    Google Scholar 

  • Brown, J. H. Why are there so many species in the tropics? J. Biogeogr. 41, 8–22 (2014).

    PubMed 
    Article 

    Google Scholar 

  • LaManna, J. A. et al. Plant diversity increases with the strength of negative density dependence at the global scale. Science 356, 1389–1392 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Bagchi, R. et al. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506, 85–88 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Lapebie, P., Lombard, V., Drula, E., Terrapon, N. & Henrissat, B. Bacteroidetes use thousands of enzyme combinations to break down glycans. Nat. Commun. https://doi.org/10.1038/s41467-019-10068-5 (2019).

  • Makhalanyane, T. P. et al. Microbial ecology of hot desert edaphic systems. FEMS Microbiol. Rev. 39, 203–221 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Aydogan, E. L., Moser, G., Muller, C., Kampfer, P. & Glaeser, S. P. Long-term warming shifts the composition of bacterial communities in the phyllosphere of Galium album in a permanent grassland field-experiment. Front. Microbiol. https://doi.org/10.3389/fmicb.2018.00144 (2018).

  • Hu, D. Y., Zang, Y., Mao, Y. J. & Gao, B. L. Identification of molecular markers that are specific to the class thermoleophilia. Front. Microbiol. https://doi.org/10.3389/fmicb.2019.01185 (2019).

  • Mohan, J. E. et al. Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: mini-review. Fungal Ecol. 10, 3–19 (2014).

    Article 

    Google Scholar 

  • Manzoni, S., Taylor, P., Richter, A., Porporato, A. & Agren, G. I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 196, 79–91 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 3, 336–340 (2010).

    CAS 
    Article 

    Google Scholar 

  • Reed, S. C. et al. Soil biogeochemical responses of a tropical forest to warming and hurricane disturbance. Adv. Ecol. Res. 62, 225–252 (2020).

    Article 

    Google Scholar 

  • Nottingham, A. T., Turner, B. L., Stott, A. W. & Tanner, E. V. J. Nitrogen and phosphorus constrain labile and stable carbon turnover in lowland tropical forest soils. Soil Biol. Biochem. 80, 26–33 (2015).

    CAS 
    Article 

    Google Scholar 

  • Walker, T. W. N. et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nat. Clim. Change 8, 885–889 (2018).

  • Kemmitt, S. J. et al. Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass—a new perspective. Soil Biol. Biochem. 40, 61–73 (2008).

    CAS 
    Article 

    Google Scholar 

  • Nannipieri, P., Trasar-Cepeda, C. & Dick, R. P. Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol. Fert. Soils 54, 11–19 (2018).

    CAS 
    Article 

    Google Scholar 

  • Wallenstein, M., Allison, S., Ernakovich, J., Steinweg, J. M. & Sinsabaugh, R. in Soil Enzymology. Soil Biology Vol. 22 (eds Shukla, G. & Varma, A.) Ch. 13 (Springer, 2011).

  • Zhou, X. Y., Chen, L., Xu, J. M. & Brookes, P. C. Soil biochemical properties and bacteria community in a repeatedly fumigated-incubated soil. Biol. Fert. Soils 56, 619–631 (2020).

    CAS 
    Article 

    Google Scholar 

  • Sanchez-Julia, M. & Turner, B. L. Abiotic contribution to phenol oxidase activity across a manganese gradient in tropical forest soils. Biogeochemistry https://doi.org/10.1007/s10533-021-00764-0 (2021).

  • Razavi, B. S., Liu, S. B. & Kuzyakov, Y. Hot experience for cold-adapted microorganisms: temperature sensitivity of soil enzymes. Soil Biol. Biochem. 105, 236–243 (2017).

    CAS 
    Article 

    Google Scholar 

  • Pinney, M. M. et al. Parallel molecular mechanisms for enzyme temperature adaptation. Science 371, eaay2784 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Fanin, N. et al. Soil enzymes in response to climate warming: mechanisms and feedbacks. Funct. Ecol. https://doi.org/10.1111/1365-2435.14027 (2022).

  • Hall, S. J. & Silver, W. L. Iron oxidation stimulates organic matter decomposition in humid tropical forest soils. Glob. Change Biol. 19, 2804–2813 (2013).

    Article 

    Google Scholar 

  • Freeman, C., Ostle, N. & Kang, H. An enzymic ‘latch’ on a global carbon store. Nature 409, 149 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Sarmiento, C. et al. Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest. Proc. Natl Acad. Sci. USA 114, 11458–11463 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Condit, R., Perez, R., Lao, S., Aguilar, S. & Hubbell, S. P. Demographic trends and climate over 35 years in the Barro Colorado 50 ha plot. For. Ecosyst. https://doi.org/10.1186/s40663-017-0103-1 (2017).

  • Woodring, W. P. Geology of Barro Colorado Island. Smithson. Misc. Collect. 135, 1–39 (1958).

    Google Scholar 

  • Sanchez, P. A. & Logan, T. J. Myths and science about the chemistry and fertility of soils in the tropics. SSSA Spec. Publ. 29, 35–46 (1992).

    CAS 

    Google Scholar 

  • Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Brookes, P. C., Landman, A., Pruden, G. & Jenkinson, D. S. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 17, 837–842 (1985).

    CAS 
    Article 

    Google Scholar 

  • Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).

    CAS 
    Article 

    Google Scholar 

  • Jenkinson, D. S., Brookes, P. C. & Powlson, D. S. Measuring soil microbial biomass. Soil Biol. Biochem. 36, 5–7 (2004).

    CAS 
    Article 

    Google Scholar 

  • Kouno, K., Tuchiya, Y. & Ando, T. Measurement of soil microbial biomass phosphorus by an anion-exchange membrane method. Soil Biol. Biochem. 27, 1353–1357 (1995).

    CAS 
    Article 

    Google Scholar 

  • Tabatabai, M. A. in Methods of Soil Analysis. Part 2. Microbiological and Biochemical Properties (ed. Page, A.L.) 778–833 (SSSA, 1994).

  • Marx, M. C., Wood, M. & Jarvis, S. C. A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol. Biochem. 33, 1633–1640 (2001).

    CAS 
    Article 

    Google Scholar 

  • Price, N. & Stevens, L. Fundamentals of Enzymology: Cell and Molecular Biology of Catalytic Proteins (Oxford Univ. Press, 1999).

  • Hagerty, S. B., Allison, S. D. & Schimel, J. P. Evaluating soil microbial carbon use efficiency explicitly as a function of cellular processes: implications for measurements and models. Biogeochemistry 140, 269–283 (2018).

    CAS 
    Article 

    Google Scholar 

  • Frey, S. D., Lee, J., Melillo, J. M. & Six, J. The temperature response of soil microbial efficiency and its feedback to climate. Nat. Clim. Change 3, 395–398 (2013).

    CAS 
    Article 

    Google Scholar 

  • Spohn, M. et al. Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland. Soil Biol. Biochem. 97, 168–175 (2016).

    CAS 
    Article 

    Google Scholar 

  • Sinsabaugh, R. L. et al. Stoichiometry of microbial carbon use efficiency in soils. Ecol. Monogr. 86, 172–189 (2016).

    Article 

    Google Scholar 

  • Geyer, K. M., Dijkstra, P., Sinsabaugh, R. & Frey, S. D. Clarifying the interpretation of carbon use efficiency in soil through methods comparison. Soil Biol. Biochem. 128, 79–88 (2019).

    CAS 
    Article 

    Google Scholar 

  • Bååth, E., Pettersson, M. & Söderberg, K. H. Adaptation of a rapid and economical microcentrifugation method to measure thymidine and leucine incorporation by soil bacteria. Soil Biol. Biochem. 33, 1571–1574 (2001).

    Article 

    Google Scholar 

  • Bárcenas-Moreno, G., Gomez-Brandon, M., Rousk, J. & Bååth, E. Adaptation of soil microbial communities to temperature: comparison of fungi and bacteria in a laboratory experiment. Glob. Change Biol. 15, 2950–2957 (2009).

    Article 

    Google Scholar 

  • Smirnova, E., Huzurbazar, S. & Jafari, F. PERFect: PERmutation Filtering test for microbiome data. Biostatistics 20, 615–631 (2019).

    PubMed 
    Article 

    Google Scholar 

  • Alberdi, A. & Gilbert, M. T. P. hilldiv: an R package for the integral analysis of diversity based on Hill numbers. Preprint at bioRxiv https://doi.org/10.1101/545665 (2019).

  • Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J. & Knight, R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 5, 169–172 (2011).

    PubMed 
    Article 

    Google Scholar 

  • Oksanen, J. et al. vegan: Community ecology package, R Package version 2 https://cran.r-project.org/web/packages/vegan/ (2018).

  • Dufrene, M. & Legendre, P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366 (1997).

    Google Scholar 

  • Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. https://doi.org/10.1186/gb-2011-12-6-r60 (2011).

  • Roesch, L. F. W. et al. PIME: a package for discovery of novel differences among microbial communities. Mol. Ecol. Resour. 20, 415–428 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Roberts, D.W. labdsv: Ordination and multivariate analysis for ecology. R package version 2.0-1 https://cran.r-project.org/web/packages/labdsv/ (2019).

  • Cao, Y. et al. microbiomeMarker: an R/Bioconductor package for microbiome marker identification and visualization. Bioinformatics 38, 4027–4029 (2022).

  • Eren, A. M. et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. Peerj 3, e1319 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Peterson, R. A. & Cavanaugh, J. E. Ordered quantile normalization: a semiparametric transformation built for the cross-validation era. J. Appl. Stat. 47, 2312–2327 (2020).

    PubMed 
    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    A harmonized dataset of sediment diatoms from hundreds of lakes in the northeastern United States

    Fission in a colonial marine invertebrate signifies unique life history strategies rather than being a demographic trait