Soil ammonia-oxidizing archaea in alpine grasslands exhibit the highest temperature sensitivity in northern Chinese grasslands

Sixue Chen , Shuang Pang , Yichen Zhu , Zonghao Hu , Yiheng Tao , Changhui Wang , Huili Jia , Ximei Zhang

Soil Ecology Letters ›› 2026, Vol. 8 ›› Issue (3) : 260405

PDF (3639KB)
Soil Ecology Letters ›› 2026, Vol. 8 ›› Issue (3) :260405 DOI: 10.1007/s42832-026-0405-8
RESEARCH ARTICLE
Soil ammonia-oxidizing archaea in alpine grasslands exhibit the highest temperature sensitivity in northern Chinese grasslands
Author information +
History +
PDF (3639KB)

Abstract

Ammonia-oxidizing archaea (AOA) are key drivers of soil nitrification, but how they respond to climate warming across northern China’s diverse grassland types remains unclear. To address this, we analyzed 88 soil samples from 22 sites across three northern China grassland biomes based on metagenomic data, quantifying AOA temperature sensitivity as the regression slope of diversity indicators against mean annual temperature (MAT). Our results revealed MAT as the key factor influencing the relative abundance, richness, and composition of the potential AOA community. In alpine grassland, AOA communities exhibited the highest temperature sensitivity, with the steepest slopes of community composition and relative abundance, and a unique decrease in richness. This high sensitivity may reduce the AOA community diversity and destabilize nitrogen cycling in alpine grasslands. Structural equation modeling indicated that MAT impacted AOA communities via a direct route rather than indirect routes. These findings provide a scientific basis for assessing the potential risks of climate warming on grassland nitrogen cycling and informing early-warning and management strategies.

Graphical abstract

Keywords

nitrogen cycling / ammonia-oxidizing archaea / temperature sensitivity / alpine grassland / climate warming / soil microbial community

Highlight

● MAT is the key factor influencing AOA communities in northern Chinese grasslands.

● MAT impacts AOA communities mainly through direct effects.

● AOA in alpine grassland soil exhibits the highest temperature sensitivity.

● AOA richness responds negatively to temperature exclusively in alpine grasslands.

Cite this article

Download citation ▾
Sixue Chen, Shuang Pang, Yichen Zhu, Zonghao Hu, Yiheng Tao, Changhui Wang, Huili Jia, Ximei Zhang. Soil ammonia-oxidizing archaea in alpine grasslands exhibit the highest temperature sensitivity in northern Chinese grasslands. Soil Ecology Letters, 2026, 8(3): 260405 DOI:10.1007/s42832-026-0405-8

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Abby, S.S., Kerou, M., Schleper, C., 2020. Ancestral reconstructions decipher major adaptations of ammonia-oxidizing archaea upon radiation into moderate terrestrial and marine environments. mBio11, e02371–20.

[2]

Allison, S.D., Martiny, J.B.H., 2008. Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences of the United States of America105 Suppl 1, 11512–11519.

[3]

Alves, R.J.E., Kerou, M., Zappe, A., Bittner, R., Abby, S.S., Schmidt, H.A., Pfeifer, K., Schleper, C., 2019. Ammonia oxidation by the arctic terrestrial thaumarchaeote Candidatus nitrosocosmicus arcticus is stimulated by increasing temperatures. Frontiers in Microbiology10, 1571.

[4]

Alves, R.J.E., Wanek, W., Zappe, A., Richter, A., Svenning, M.M., Schleper, C., Urich, T., 2013. Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea. The ISME Journal7, 1620–1631.

[5]

Bahram, M., Hildebrand, F., Forslund, S.K., Anderson, J.L., Soudzilovskaia, N.A., Bodegom, P.M., Bengtsson-Palme, J., Anslan, S., Coelho, L.P., Harend, H., Huerta-Cepas, J., Medema, M.H., Maltz, M.R., Mundra, S., Olsson, P.A., Pent, M., Põlme, S., Sunagawa, S., Ryberg, M., Tedersoo, L., Bork, P., 2018. Structure and function of the global topsoil microbiome. Nature560, 233–237.

[6]

Bale, N.J., Palatinszky, M., Rijpstra, W.I.C., Herbold, C.W., Wagner, M., Sinninghe Damsté, J.S., 2019. Membrane lipid composition of the moderately thermophilic ammonia-oxidizing archaeon "Candidatus Nitrosotenuis uzonensis" at different growth temperatures. Applied and Environmental Microbiology85, e01332–19.

[7]

Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software67, 1–48.

[8]

Broadbent, A.A.D., Snell, H.S.K., Michas, A., Pritchard, W.J., Newbold, L., Cordero, I., Goodall, T., Schallhart, N., Kaufmann, R., Griffiths, R.I., Schloter, M., Bahn, M., Bardgett, R.D., 2021. Climate change alters temporal dynamics of alpine soil microbial functioning and biogeochemical cycling via earlier snowmelt. The ISME Journal15, 2264–2275.

[9]

Buchfink, B., Xie, C., Huson, D.H., 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods12, 59–60.

[10]

Cai, M.K., Zhang, Y.J., Zhao, G., Zhao, B., Cong, N., Zhu, J.T., Zheng, Z.T., Wu, W.J., Duan, X.Q., 2024. Excessive climate warming exacerbates nitrogen limitation on microbial metabolism in an alpine meadow of the Tibetan Plateau: evidence from soil ecoenzymatic stoichiometry. Science of the Total Environment930, 172731.

[11]

Cao, H.L., Auguet, J.C., Gu, J.D., 2013. Global ecological pattern of ammonia-oxidizing archaea. PLoS One8, e52853.

[12]

Chen, J.S., Chiu, C.Y., 2003. Characterization of soil organic matter in different particle-size fractions in humid subalpine soils by CP/MAS 13C NMR. Geoderma117, 129–141.

[13]

Chen, S.F., Zhou, Y.Q., Chen, Y.R., Gu, J., 2018. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics34, i884–i890.

[14]

Chen, Y., Qin, W.K., Zhang, Q.F., Wang, X.D., Feng, J.G., Han, M.G., Hou, Y.H., Zhao, H.Y., Zhang, Z.H., He, J.S., Torn, M.S., Zhu, B., 2024. Whole-soil warming leads to substantial soil carbon emission in an alpine grassland. Nature Communications15, 4489.

[15]

Daims, H., Lebedeva, E.V., Pjevac, P., Han, P., Herbold, C., Albertsen, M., Jehmlich, N., Palatinszky, M., Vierheilig, J., Bulaev, A., Kirkegaard, R.H., von Bergen, M., Rattei, T., Bendinger, B., Nielsen, P.H., Wagner, M., 2015. Complete nitrification by Nitrospira bacteria. Nature528, 504–509.

[16]

Dong, S.K., 2023. Revitalizing the grassland on the Qinghai-Tibetan Plateau. Grassland Research2, 241–250.

[17]

Duan, P.P., Wu, Z., Zhang, Q.Q., Fan, C.H., Xiong, Z.Q., 2018. Thermodynamic responses of ammonia-oxidizing archaea and bacteria explain N2O production from greenhouse vegetable soils. Soil Biology and Biochemistry120, 37–47.

[18]

Fay, P.A., Prober, S.M., Harpole, W.S., Knops, J.M.H., Bakker, J.D., Borer, E.T., Lind, E.M., MacDougall, A.S., Seabloom, E.W., Wragg, P.D., Adler, P.B., Blumenthal, D.M., Buckley, Y.M., Chu, C.J., Cleland, E.E., Collins, S.L., Davies, K.F., Du, G.Z., Feng, X.H., Firn, J., Gruner, D.S., Hagenah, N., Hautier, Y., Heckman, R.W., Jin, V.L., Kirkman, K.P., Klein, J., Ladwig, L.M., Li, Q., Mcculley, R.L., Melbourne, B.A., Mitchell, C.E., Moore, J.L., Morgan, J.W., Risch, A.C., Schütz, M., Stevens, C.J., Wedin, D.A., Yang, L.H., 2015. Grassland productivity limited by multiple nutrients. Nature Plants1, 15080.

[19]

Feng, J.G., Wang, J.S., Song, Y.J., Zhu, B., 2018. Patterns of soil respiration and its temperature sensitivity in grassland ecosystems across China. Biogeosciences15, 5329–5341.

[20]

Fox, J., Weisberg, S., 2019. An R companion to applied regression, third edition. Available at the website of john-fox.ca/Companion/

[21]

Frey, B., Moser, B., Tytgat, B., Zimmermann, S., Alberti, J., Biederman, L.A., Borer, E.T., Broadbent, A.A.D., Caldeira, M.C., Davies, K.F., Eisenhauer, N., Eskelinen, A., Fay, P.A., Hagedorn, F., Hautier, Y., MacDougall, A.S., McCulley, R.L., Moore, J.L., Nepel, M., Power, S.A., Seabloom, E.W., Vázquez, E., Virtanen, R., Yahdjian, L., Risch, A.C., 2023. Long-term N-addition alters the community structure of functionally important N-cycling soil microorganisms across global grasslands. Soil Biology and Biochemistry176, 108887.

[22]

Frindte, K., Pape, R., Werner, K., Löffler, J., Knief, C., 2019. Temperature and soil moisture control microbial community composition in an arctic–alpine ecosystem along elevational and micro-topographic gradients. The ISME Journal13, 2031–2043.

[23]

Gemayel, K., Lomsadze, A., Borodovsky, M., 2022. MetaGeneMark-2: improved gene prediction in metagenomes. https://doi.org/10.1101/2022.07.25.500264.

[24]

Ghoul, M., Mitri, S., 2016. The ecology and evolution of microbial competition. Trends in Microbiology24, 833–845.

[25]

Hedley, M.J., Stewart, J.W.B., Chauhan, B.S., 1982. Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Science Society of America Journal46, 970–976.

[26]

Hu, H.W., Zhang, L.M., Dai, Y., Di, H.J., He, J.Z., 2013. pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. Journal of Soils and Sediments13, 1439–1449.

[27]

Hu, S., Zhou, T.J., Wu, B., 2025. Accelerated warming of High Mountain Asia predicted at multiple years ahead. Science Bulletin70, 419–428.

[28]

IPCC, 2023. Climate Change 2023: Synthesis Report, Summary for Policymakers. Contribution of Working Groups I, II and III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC35–115.

[29]

Jones, D., Willett, V., 2006. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biology and Biochemistry38, 991–999.

[30]

Jung, M.Y., Well, R., Min, D., Giesemann, A., Park, S.J., Kim, J.G., Kim, S.J., Rhee, S.K., 2014. Isotopic signatures of N2O produced by ammonia-oxidizing archaea from soils. The ISME Journal8, 1115–1125.

[31]

Kuypers, M.M.M., Marchant, H.K., Kartal, B., 2018. The microbial nitrogen-cycling network. Nature Reviews Microbiology16, 263–276.

[32]

Lai, J.S., Zou, Y., Zhang, S., Zhang, X.G., Mao, L.F., 2022. glmm. hp: an R package for computing individual effect of predictors in generalized linear mixed models. Journal of Plant Ecology15, 1302–1307.

[33]

LeBauer, D.S., Treseder, K.K., 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology89, 371–379.

[34]

Lefcheck, J.S., 2016. PIECEWISESEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods in Ecology and Evolution7, 573–579.

[35]

Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G.W., Prosser, J.I., Schuster, S.C., Schleper, C., 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature442, 806–809.

[36]

Lenth, R.V., 2025. Emmeans: estimated marginal means, aka least-squares means. Available at the website of rvlenth.github.io/emmeans/.

[37]

Li, C.Y., He, Z.Y., Hu, H.W., He, J.Z., 2023. Niche specialization of comammox Nitrospira in terrestrial ecosystems: oligotrophic or copiotrophic. Critical Reviews in Environmental Science and Technology53, 161–176.

[38]

Li, D.H., Luo, R.B., Liu, C.M., Leung, C.M., Ting, H.F., Sadakane, K., Yamashita, H., Lam, T.W., 2016. MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods102, 3–11.

[39]

Li, L.H., Chen, J.Q., Han, X.G., Zhang, W.H., Shao, C.L., 2020. Types and distribution of Chinese grassland ecosystems. In: Li, L.H., Chen, J.Q., Han, X.G., Zhang, W.H., Shao, C.L., eds. Grassland Ecosystems of China: A Synthesis and Resume. Singapore: Springer121–147.

[40]

Magalhães, C.M., Machado, A., Frank-Fahle, B., Lee, C.K., Cary, S.C., 2014. The ecological dichotomy of ammonia-oxidizing archaea and bacteria in the hyper-arid soils of the Antarctic Dry Valleys. Frontiers in Microbiology5, 515.

[41]

Martens-Habbena, W., Berube, P.M., Urakawa, H., de la Torre, J.R., Stahl, D.A., 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature461, 976–979.

[42]

Nicol, G.W., Leininger, S., Schleper, C., Prosser, J.I., 2008. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology10, 2966–2978.

[43]

Oksanen, J., Simpson, G., Blanchet, F., Kindt, R., Legendre, P., Minchin, P., O'Hara, R., Solymos, P., 2022. vegan community ecology package version 2.6-2 April 2022. Available at the website of CRAN.R-project.org/package=vegan.

[44]

Ouyang, Y., Norton, J.M., Stark, J.M., 2017. Ammonium availability and temperature control contributions of ammonia oxidizing bacteria and archaea to nitrification in an agricultural soil. Soil Biology and Biochemistry113, 161–172.

[45]

Picazo, F., Vilmi, A., Aalto, J., Soininen, J., Casamayor, E.O., Liu, Y.Q., Wu, Q.L., Ren, L.J., Zhou, J.Z., Shen, J., Wang, J.J., 2020. Climate mediates continental scale patterns of stream microbial functional diversity. Microbiome8, 92.

[46]

Prosser, J.I., Nicol, G.W., 2012. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends in Microbiology20, 523–531.

[47]

Qin, W., Wei, S.P., Zheng, Y., Choi, E., Li, X.P., Johnston, J., Wan, X.H, Abrahamson, B., Flinkstrom, Z., Wang, B.Z., Li, H.Y., Hou, L., Tao, Q., Chlouber, W.W., Sun, X., Wells, M., Ngo, L., Hunt, K.A., Urakawa, H., Tao, X.Y., Wang, D.Y., Yan, X.Y., Wang, D.Z., Pan, C., Weber, P.K., Jiang, J.D., Zhou, J.Z., Zhang, Y., Stahl, D.A., Ward, B.B., Mayali, X., Martens-Habbena, W., Winkler, M.K.H., 2024. Ammonia-oxidizing bacteria and archaea exhibit differential nitrogen source preferences. Nature Microbiology9, 524–536.

[48]

R Core Team., 2024. R: a language and environment for statistical computing. Available at the website of cran.rstudio.com/manuals.html.

[49]

Rattanasriampaipong, R., Zhang, Y.G., Pearson, A., Hedlund, B.P., Zhang, S., 2022. Archaeal lipids trace ecology and evolution of marine ammonia-oxidizing archaea. Proceedings of the National Academy of Sciences of the United States of America119, e2123193119.

[50]

Reich, P.B., Mohanbabu, N., Isbell, F., Hobbie, S.E., Butler, E.E., 2024. High CO2 dampens then amplifies N-induced diversity loss over 24 years. Nature635, 370–375.

[51]

Shen, W., Le, S., Li, Y., Hu, F.Q., 2016. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS One11, e0163962.

[52]

Shi, Y.J., Religieux, E., Kuzyakov, Y., Wang, J.F., Hu, J.X., Le Roux, X., 2023. Local climate conditions explain the divergent climate change effects on (de)nitrification across the grassland biome: a meta-analysis. Soil Biology and Biochemistry187, 109218.

[53]

Stieglmeier, M., Mooshammer, M., Kitzler, B., Wanek, W., Zechmeister-Boltenstern, S., Richter, A., Schleper, C., 2014. Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. The ISME Journal8, 1135–1146.

[54]

Tu, Q.C., Lin, L., Cheng, L., Deng, Y., He, Z.L., 2019. NCycDB: a curated integrative database for fast and accurate metagenomic profiling of nitrogen cycling genes. Bioinformatics35, 1040–1048.

[55]

Walker, J.K.M., Egger, K.N., Henry, G.H.R., 2008. Long-term experimental warming alters nitrogen-cycling communities but site factors remain the primary drivers of community structure in high arctic tundra soils. The ISME Journal2, 982–995.

[56]

Wang, L., Delgado-Baquerizo, M., Wang, D.L., Isbell, F., Liu, J., Feng, C., Liu, J.S., Zhong, Z.W., Zhu, H., Yuan, X., Chang, Q., Liu, C., 2019. Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proceedings of the National Academy of Sciences of the United States of America116, 6187–6192.

[57]

Wang, X.B., Lü, X.T., Yao, J., Wang, Z.W., Deng, Y., Cheng, W.X., Zhou, J.Z., Han, X.G., 2017. Habitat-specific patterns and drivers of bacterial β-diversity in China’s drylands. The ISME Journal11, 1345–1358.

[58]

Wang, Y.N., Zeng, X.B., Ma, Q., Zhang, Y., Yu, W.T., Zheng, Z., Zhang, N., Xu, L.Y., 2023. Differential responses of canonical nitrifiers and comammox Nitrospira to long-term fertilization in an Alfisol of Northeast China. Frontiers in Microbiology14, 1095937.

[59]

Xiao, R., Qiu, Y.P., Tao, J.J., Zhang, X.L., Chen, H.H., Reberg-Horton, S.C., Shi, W., Shew, H.D., Zhang, Y., Hu, S.J., 2020. Biological controls over the abundances of terrestrial ammonia oxidizers. Global Ecology and Biogeography29, 384–399.

[60]

Yang, W., Chen, H.H., Chen, Y.F., Chen, A.P., Feng, X., Zhao, B., Zheng, F.F., Fang, H.W., Zhang, C.Y., Zeng, Z.R., 2023. Thermophilic archaeon orchestrates temporal expression of GDGT ring synthases in response to temperature and acidity stress. Environmental Microbiology25, 575–587.

[61]

Zhang, Y.W., Zhang, Y.L., Huo, T.C., Wei, B., Chen, K.L., Liu, N., Zhang, Y.J., Liang, J.Y., 2022. Vegetation restoration constrained by nitrogen availability in temperate grasslands in northern China. Journal of Plant Ecology16, rtac087.

[62]

Zhao, Y.W., Ling, N., Liu, X., Li, C., Jing, X., Hu, J.J., Rui, J.P., 2024. Altitudinal patterns of alpine soil ammonia-oxidizing community structure and potential nitrification rate. Applied and Environmental Microbiology90, e00070–24.

RIGHTS & PERMISSIONS

Higher Education Press

PDF (3639KB)

Supplementary files

Supplementary materials

253

Accesses

0

Citation

Detail

Sections
Recommended

/