Grazing intensity is associated with shifts in nutrient status, metabolite profiles, and selected bacterial taxa in biological soil crusts

Jiangping Gao , Zengru Wang , Yubing Liu

Soil Ecology Letters ›› 2027, Vol. 9 ›› Issue (2) : 260521

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Soil Ecology Letters ›› 2027, Vol. 9 ›› Issue (2) :260521 DOI: 10.1007/s42832-026-0521-5
RESEARCH ARTICLE
Grazing intensity is associated with shifts in nutrient status, metabolite profiles, and selected bacterial taxa in biological soil crusts
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Abstract

Grazing can alter bacterial communities by influencing soil properties and metabolites. Nevertheless, metabolites in biological soil crusts (BSCs) under grazing disturbance remain poorly understood. Here, we collected BSC samples under three grazing intensities (0 [enclosure, EN], 1.00 [light grazing, LG], and 2.33 [heavy grazing, HG] sheep-units ha−1 year−1) in the arid region of northwestern China to explore the effects of physicochemical properties and metabolites on bacterial communities. Our results indicated that the number of metabolites decreased with increasing grazing intensity, which markedly altered metabolite composition. Nutrients (NO3−-N and NH4+-N) and the metabolite composition of BSCs were closely correlated with bacterial community composition (p < 0.05). A total of 135, 131, and 124 differential metabolites were identified between the EN and LG, EN and HG, and LG and HG groups, among which organic oxygen compounds, phenylpropanoids and polyketides, and lipids and lipid-like molecules were the major classes. Co-occurrence network analysis revealed significant correlations between major differential metabolites and dominant bacteria (Proteobacteria, Actinobacteriota, and Chloroflexi). These results highlight that nutrients and metabolites in BSCs play important roles in regulating bacterial community composition, providing data support for the conservation and restoration of desert grasslands.

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Keywords

biological soil crusts / grazing intensity / bacterial community composition / differential metabolites / soil nutrients

Highlight

● Increasing grazing intensity decreased metabolite count and altered metabolite composition in BSCs.

● Grazing intensity did not affect bacterial community diversity but induced adaptive shifts in bacterial community composition.

● BSCs nutrients and metabolites were significantly correlated with bacterial community composition.

● Abundant differential metabolites occurred across grazing gradients, with the most complex co-occurrence network between enclosure and heavy grazing.

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Jiangping Gao, Zengru Wang, Yubing Liu. Grazing intensity is associated with shifts in nutrient status, metabolite profiles, and selected bacterial taxa in biological soil crusts. Soil Ecology Letters, 2027, 9 (2) : 260521 DOI:10.1007/s42832-026-0521-5

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References

[1]

Akiyama, H., Yan, X.Y., Yagi, K., 2010. Evaluation of effectiveness of enhanced-efficiency fertilizers as mitigation options for N2O and NO emissions from agricultural soils: meta-analysis. Global Change Biology16, 1837–1846.

[2]

Badri, D.V., Vivanco, J.M., 2009. Regulation and function of root exudates. Plant, Cell & Environment32, 666–681.

[3]

Bakker, P.A.H.M., Pieterse, C.M.J., de Jonge, R., Berendsen, R.L., 2018. The soil-borne legacy. Cell172, 1178–1180.

[4]

Bao, S.D., 2000. Analysis Method of Soil Agricultural Chemistry. 3rd ed. Beijing: China Agricultural Press.

[5]

Bastian, M., Heymann, S., Jacomy, M., 2009. Gephi: an open source software for exploring and manipulating networks. In: Proceedings of the 3rd International AAAI Conference on Web and Social Media. San Jose: AAAI, 361–362.

[6]

Belnap, J., 2006. The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrological Processes20, 3159–3178.

[7]

Bethany, J., Giraldo-Silva, A., Nelson, C., Barger, N.N., Garcia-Pichel, F., 2019. Optimizing the production of nursery-based biological soil crusts for restoration of arid land soils. Applied and Environmental Microbiology85, e00735–19.

[8]

Bi, B.Y., Yuan, Y., Zhang, H., Wu, Z.H., Wang, Y., Han, F.P., 2022. Rhizosphere soil metabolites mediated microbial community changes of Pinus sylvestris var. mongolica across stand ages in the Mu Us Desert. Applied Soil Ecology169, 104222.

[9]

Camuy-Vélez, L.A., Banerjee, S., Sedivec, K., 2024. Grazing intensity alters network complexity and predator–prey relationships in the soil microbiome. Applied and Environmental Microbiology90, e00425–24.

[10]

Chandel, N.S., 2021. Lipid metabolism. Cold Spring Harbor Perspectives in Biology13, a040576.

[11]

Chen, Y., Qiu, Y., Hao, X.M., Tong, L., Li, S.E., Kang, S.Z., 2023. Does biochar addition improve soil physicochemical properties, bacterial community and alfalfa growth for saline soils. Land Degradation & Development34, 3314–3328.

[12]

Cotton, T. A., Pétriacq, P., Cameron, D. D., Meselmani, M. A., Schwarzenbacher, R., Rolfe, S. A., Ton, J., 2019. Metabolic regulation of the maize rhizobiome by benzoxazinoids. The ISME journal13, 1647–1658.

[13]

Czaban, W., Rasmussen, J., Laursen, B.B., Vidkjær, N.H., Sapkota, R., Nicolaisen, M., Fomsgaard, I.S., 2018. Multiple effects of secondary metabolites on amino acid cycling in white clover rhizosphere. Soil Biology and Biochemistry123, 54–63.

[14]

Deng, L., Li, J.W., Qu, Q., Shi, J.W., Shangguan, Z.P., 2024. Dynamics and driving mechanisms of soil organic carbon sequestration in grasslands after grazing exclusion: a review. Chinese Journal of Applied Ecology35, 3208–3216.

[15]

Ding, X.W., Liu, K.H., Yan, Q.Y., Liu, X.Y., Chen, N., Wang, G.L., He, S., 2021. Sugar and organic acid availability modulate soil diazotroph community assembly and species co-occurrence patterns on the Tibetan Plateau. Applied Microbiology and Biotechnology105, 8545–8560.

[16]

Du, H.B., Wang, B.T., Dawood, M., Qu, P., Li, W.F., Zhang, L.Y., Bukhari, S.A.H., Shi, X.D., Qi, M.J., Dong, S.L., Ge, Y., 2025. Root diameter-associated exudates drive the changes in rhizosphere microbial communities. Journal of Soil Science and Plant Nutrition25, 2438–2450.

[17]

Du, Y.G., Ke, X., Guo, X.W., Cao, G.M., Zhou, H.K., 2019. Soil and plant community characteristics under long-term continuous grazing of different intensities in an alpine meadow on the Tibetan plateau. Biochemical Systematics and Ecology85, 72–75.

[18]

Garcia-Pichel, F., 2023. The microbiology of biological soil crusts. Annual Review of Microbiology77, 149–171.

[19]

Hu, L.F., Robert, C.A.M., Cadot, S., Zhang, X., Ye, M., Li, B.B., Manzo, D., Chervet, N., Steinger, T., van der Heijden, M.G.A., Schlaeppi, K., Erb, M., 2018. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nature Communications9, 2738.

[20]

Huang, L.B., Bai, J.H., Wang, J.J., Zhang, G.L., Wang, W., Wang, X., Zhang, L., Wang, Y.Q., Liu, X.H., Cui, B.S., 2022. Different stochastic processes regulate bacterial and fungal community assembly in estuarine wetland soils. Soil Biology and Biochemistry167, 108586.

[21]

Jia, R.L., Teng, J.L., Chen, M.C., Zhao, Y., Gao, Y.H., 2018. The differential effects of sand burial on CO2, CH4, and N2O fluxes from desert biocrust-covered soils in the Tengger Desert, China. Catena160, 252–260.

[22]

Khan, A., Kanwal, F., Ullah, S., Fahad, M., Tariq, L., Altaf, M.T., Riaz, A., Zhang, G.P., 2025. Plant secondary metabolites—central regulators against abiotic and biotic stresses. Metabolites15, 276.

[23]

Kurtz, Z.D., Müller, C.L., Miraldi, E.R., Littman, D.R., Blaser, M.J., Bonneau, R.A., 2015. Sparse and compositionally robust inference of microbial ecological networks. PLoS Computational Biology11, e1004226.

[24]

Li, P.Z., Zhang, Z.H., Dong, Y., Guo, C.T., Rong, Y.P., 2025. Mixed grazing of lambs and ewes improves lamb growth performance by reducing foraging time and activity-related energy expenditure. Journal of Environmental Management396, 128075.

[25]

Li, W., Ma, X.X., Ma, N., Zhao, Y.G., Qiao, Y., Wang, P., Sun, H., 2021. Effects of grazing intensity on stoichiomerty of biological soil crusts in the hilly Loess Plateau region. Acta Agrestia Sinica29, 2547–2555.

[26]

Li, Z.K., Shen, Y., Zhang, W.Y., Zhang, H., Liu, L.J., Wang, Z.Q., Gu, J.F., Yang, J.C., 2023. Effects of long-term straw returning on rice yield and soil properties and bacterial community in a rice-wheat rotation system. Field Crops Research291, 108800.

[27]

Liu, Y.B., Zhao, L.N., Wang, Z.R., Liu, L.C., Zhang, P., Sun, J.Y., Wang, B.Y., Song, G., Li, X.R., 2018. Changes in functional gene structure and metabolic potential of the microbial community in biological soil crusts along a revegetation chronosequence in the Tengger Desert. Soil Biology and Biochemistry126, 40–48.

[28]

Mager, D.M., 2010. Carbohydrates in cyanobacterial soil crusts as a source of carbon in the southwest Kalahari, Botswana. Soil Biology and Biochemistry42, 313–318.

[29]

Mallen-Cooper, M., Eldridge, D.J., Delgado-Baquerizo, M., 2018. Livestock grazing and aridity reduce the functional diversity of biocrusts. Plant and Soil429, 175–185.

[30]

Morriën, E., Hannula, S.E., Snoek, L.B., Helmsing, N.R., Zweers, H., de Hollander, M., Soto, R.L., Bouffaud, M.L., Buée, M., Dimmers, W., Duyts, H., Geisen, S., Girlanda, M., Griffiths, R.I., Jørgensen, H.B., Jensen, J., Plassart, P., Redecker, D., Schmelz, R.M., Schmidt, O., Thomson, B.C., Tisserant, E., Uroz, S., Winding, A., Bailey, M.J., Bonkowski, M., Faber, J.H., Martin, F., Lemanceau, P., de Boer, W., van Veen, J.A., van Der Putten, W.H., 2017. Soil networks become more connected and take up more carbon as nature restoration progresses. Nature Communications8, 14349.

[31]

Nanjing Institute of Soil Research, 1978. Analysis of Soil Physicochemical Features. Shanghai: Shanghai Science and Technology Press360.

[32]

Nelson, D.W., Sommers, L.E., 1983. Total carbon, organic carbon, and organic matter. In: Page, A.L., ed. Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties. 2nd ed. Madison: American Society of Agronomy539–577.

[33]

Ninkuu, V., Aluko, O.O., Yan, J.P., Zeng, H.M., Liu, G.D., Zhao, J., Li, H.H., Chen, S.B., Dakora, F.D., 2025. Phenylpropanoids metabolism: recent insight into stress tolerance and plant development cues. Frontiers in Plant Science16, 1571825.

[34]

Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Stevens, M.H.H., Oksanen, M.J., Suggests, M., 2007. The Vegan Package. Community Ecology Package631–637.

[35]

Pan, H., Liu, H.Y., Liu, Y.W., Zhang, Q.C., Luo, Y., Liu, X.M., Liu, Y.M., Xu, J.M., Di, H.J., Li, Y., 2018. Understanding the relationships between grazing intensity and the distribution of nitrifying communities in grassland soils. Science of the Total Environment634, 1157–1164.

[36]

Paradis, E., Claude, J., Strimmer, K., 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics20, 289–290.

[37]

Pepe-Ranney, C., Koechli, C., Potrafka, R., Andam, C., Eggleston, E., Garcia-Pichel, F., Buckley, D.H., 2016. Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation. The ISME Journal10, 287–298.

[38]

Qiao, Y.L., Xu, W.H., Kong, L.B., Shen, M.G., Wang, S., Sun, Y.D., Gao, Y., Jiang, Q., Xue, J.L., Cheng, D.L., Liu, Y.Y., 2024. Bacterial specialists playing crucial roles in maintaining system stability and governing microbial diversity in bioremediation of oil-polluted sediments under typical deep-sea condition. Bioresource Technology413, 131498.

[39]

Rivera-Aguilar, V., Montejano, G., Rodríguez-Zaragoza, S., Durán-Díaz, A., 2006. Distribution and composition of cyanobacteria, mosses and lichens of the biological soil crusts of the Tehuacán Valley, Puebla, México. Journal of Arid Environments67, 208–225.

[40]

Rong, Y.P., Monaco, T.A., Liu, Z.K., Zhao, M.L., Han, G.D., 2022. Soil microbial community structure is unaltered by grazing intensity and plant species richness in a temperate grassland steppe in northern China. European Journal of Soil Biology110, 103404.

[41]

Singh, R., Song, P., Jain, R., Chauhan, A., Kumar, R., Gunsola, D., Chattaraj, S., De Los Santos-Villalobos, S., Mitra, D., Gaur, A., 2026. Microbial metabolites—a sustainable solution for agricultural challenges: a review. Pedosphere36, 302–316.

[42]

Steven, B., Belnap, J., Kuske, C.R., 2018. Chronic physical disturbance substantially alters the response of biological soil crusts to a wetting pulse, as characterized by metatranscriptomic sequencing. Frontiers in Microbiology9, 2382.

[43]

Su, J.H., Ji, W.H., Sun, X.M., Wang, H.F., Kang, Y.K., Yao, B.H., 2023. Effects of different management practices on soil microbial community structure and function in alpine grassland. Journal of Environmental Management327, 116859.

[44]

Sun, F.H., Xiao, B., Tuller, M., 2024. Multifaceted impacts of moss-dominated biocrusts on dryland soils: from soil pore structure to aeration and water infiltration. Catena236, 107755.

[45]

Swenson, T.L., Karaoz, U., Swenson, J.M., Bowen, B.P., Northen, T.R., 2018. Linking soil biology and chemistry in biological soil crust using isolate exometabolomics. Nature Communications9, 19.

[46]

Tabeni, S., Garibotti, I.A., Pissolito, C., Aranibar, J.N., 2014. Grazing effects on biological soil crusts and their interaction with shrubs and grasses in an arid rangeland. Journal of Vegetation Science25, 1417–1425.

[47]

Vidaller, C., Malik, C., Dutoit, T., 2022. Grazing intensity gradient inherited from traditional herding still explains Mediterranean grassland characteristics despite current land-use changes. Agriculture, Ecosystems & Environment338, 108085.

[48]

Wang, L., Wang, Y.J., Sun, D.D., Wang, J.Y., Lee, S.J., Rossel, R.A.V., Gan, Y.T., 2024. Soil carbon stocks in temperate grasslands reach equilibrium with grazing duration. Science of the Total Environment949, 175081.

[49]

Wang, Y.X., Ju, X., Wu, Q., Han, G.D., 2025. Effects of grazing intensity on microbial diversity at different soil depths in desert steppe soils. Agronomy15, 124.

[50]

Wang, Y.Z., Zhang, H.F., Zhang, Y.P., Fei, J.C., Xiangmin, R., Peng, J.W., Luo, G.W., 2023. Crop rotation-driven changes in rhizosphere metabolite profiles regulate soil microbial diversity and functional capacity. Agriculture, Ecosystems & Environment358, 108716.

[51]

Weber, B., Belnap, J., Büdel, B., Antoninka, A.J., Barger, N.N., Chaudhary, V.B., Darrouzet-Nardi, A., Eldridge, D.J., Faist, A.M., Ferrenberg, S., Havrilla, C.A., Huber-Sannwald, E., Malam Issa, O., Maestre, F.T., Reed, S.C., Rodriguez-Caballero, E., Tucker, C., Young, K.E., Zhang, Y.M., Zhao, Y.G., Zhou, X.B., Bowker, M.A., 2022. What is a biocrust? A refined, contemporary definition for a broadening research community. Biological Reviews97, 1768–1785.

[52]

Yin, W.D., Zhou, L.F., Yang, K.W., Fang, J.Y., Biere, A., Callaway, R.M., Wu, M.K., Yu, H.W., Shi, Y., Ding, J.Q., 2023. Rapid evolutionary trade-offs between resistance to herbivory and tolerance to abiotic stress in an invasive plant. Ecology Letters26, 942–954.

[53]

Zhang, H.F., Luo, G.W., Wang, Y.Z., Fei, J.C., Rong, X.M., Peng, J.W., Tian, C., Zhang, Y.P., 2023. Crop rotation-driven change in physicochemical properties regulates microbial diversity, dominant components, and community complexity in paddy soils. Agriculture, Ecosystems & Environment343, 108278.

[54]

Zhang, L., Yang, J.S., Ge, A.H., Xie, W.P., Yao, R.J., Wang, X.P., 2024. Salinity drives niche differentiation of soil bacteria and archaea in Hetao Plain, China. Journal of Environmental Management370, 122977.

[55]

Zhang, X.F., Feng, Q., Cao, J.J., Liu, W., Qin, Y.Y., Zhu, M., Han, T., 2023. Grazing practices affect soil microbial networks but not diversity and composition in alpine meadows of northeastern Qinghai-Tibetan plateau. Environmental Research235, 116656.

[56]

Zhao, X., Shi, Y., Liu, Y., Jia, R.L., Li, X.R., 2015. Osmotic adjustment of soil biocrust mosses in response to desiccation stress. Pedosphere25, 459–467.

[57]

Zhao, Y., Zhao, Y.Q., Xu, W.W., Lian, Y.C., Zhang, Z.S., 2023. Are lipids, phenylpropanoids, and benzenoids potential metabolite biomarkers for succession in desert biocrusts?. Biology and Fertility of Soils59, 1013–1017.

[58]

Zhou, S.J., Dong, Y.Q., Yang, H.L., Yang, S.W., Julihaiti, A., Liu, Z.Y., Nie, T.T., Jiang, A.J., Wu, Y., An, S.Z., 2024. Effects of grazing exclusion on soil properties, fungal community structure, and diversity in different grassland types. Ecology and Evolution14, e11056.

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