Spatial variations and driving factors of soil microbial traits in healthy and unhealthy Populus euphratica along riparian gradients

Reyila Mumin , Wen Zhao , Kaichuan Huang , Long Zeng , Dongmei Wu , Neng Gao , Junning Li , Asadilla Yusup , Yifei Sun , Baokai Cui

Soil Ecology Letters ›› 2026, Vol. 8 ›› Issue (3) : 260407

PDF (4586KB)
Soil Ecology Letters ›› 2026, Vol. 8 ›› Issue (3) :260407 DOI: 10.1007/s42832-026-0407-6
RESEARCH ARTICLE
Spatial variations and driving factors of soil microbial traits in healthy and unhealthy Populus euphratica along riparian gradients
Author information +
History +
PDF (4586KB)

Abstract

Water availability and soil microbes critically influence plant survival and health in extreme desert ecosystems. Here, we investigated the dynamic changes in soil microbial traits associated with healthy and unhealthy Populus euphratica trees at varying distances from the river, while also examined the assembly mechanisms and ecological relationships between biotic and abiotic drivers. The results revealed nonlinear responses of microbial traits—including diversity, composition, functions, and network structure—to river proximity, exerting stronger effects than tree health status. Dominant and key taxa, as well as functions, differed between healthy and unhealthy trees. Mycorrhizal fungi were enriched in healthy stands, peaking at 4 km, while saprotrophic and parasitic fungi were more abundant in unhealthy stands, peaking at 6 km. Both healthy and unhealthy trees exhibited enrichment in primary bacterial functional categories—metabolism, environmental information processing, and cellular processes; however, differed in tertiary functional composition. Fungal networks were less complex than bacterial networks, though both were dominated by positive interactions. Community assembly for both fungal and bacterial communities was primarily driven by stochastic dispersal limitation. Soil available phosphorus, pH, grass cover, and litter cover were identified as critical ecological factors, regulating fungal and bacterial traits via distinct pathways. Biotic and abiotic interactions accounted for 42%‒72% of fungal and 68%‒84% of bacterial traits variation. β-diversity exhibited strong and contrasting effects on fungal and bacterial functional traits. Network intensity significantly positively influenced specific bacterial functional traits. These findings provide a theoretical foundation for understanding microbial adaptation mechanisms and ecological restoration in arid riparian forests.

Graphical abstract

Keywords

soil microbes / diversity / functions / networks / ecological drivers

Highlight

● River proximity exerted greater direct influence on microbial traits than the health status of Populus euphra tica .

● Dominant and key taxa, as well as functions, differed between healthy and unhealthy trees.

● Fungal networks were less complex than bacterial networks, though both were dominated by positive interactions and exhibited distance-dependent variations.

● Stochastic dispersal limitation primarily dictated microbial community assembly.

● Biotic and abiotic interactions accounted for 42%‒72% of fungal and 68%‒84% of bacterial traits variation.

Cite this article

Download citation ▾
Reyila Mumin, Wen Zhao, Kaichuan Huang, Long Zeng, Dongmei Wu, Neng Gao, Junning Li, Asadilla Yusup, Yifei Sun, Baokai Cui. Spatial variations and driving factors of soil microbial traits in healthy and unhealthy Populus euphratica along riparian gradients. Soil Ecology Letters, 2026, 8(3): 260407 DOI:10.1007/s42832-026-0407-6

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

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.

[2]

Banerjee, S., Walder, F., Büchi, L., Meyer, M., Held, A.Y., Gattinger, A., 2019. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in soils. Nature Communications10, 3811.

[3]

Bardgett, R.D., Mommer, L., De Vries, F.T., 2014. Going underground: root traits as drivers of ecosystem processes. Trends in Ecology & Evolution29, 692–699.

[4]

Bennett, J.A., Maherali, H., Reinhart, K.O., Lekberg, Y., Hart, M.M., Klironomos, J., 2017. Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science355, 181–184.

[5]

Berendsen, R.L., Pieterse, C.M.J., Bakker, P.A.H.M., 2012. The rhizosphere microbiome and plant health. Trends in Plant Science17, 478–486.

[6]

Busby, P.E., Soman, C., Wagner, M.R., Friesen, M.L., Kremer, J., Bennett, A., Morsy, M., Eisen, J.A., Leach, J.E., Dangl, J.L., 2017. Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biology15, e2001793.

[7]

Chen, P., Yu, K.F., He, Y.L., 2023. The dynamics and transmission of antibiotic resistance associated with plant microbiomes. Environment International176, 107986.

[8]

Chen, Y., Li, Z., Fan, Y., 2020. Hydrological and ecological responses to ecosystem restoration in the Tarim River Basin. Journal of Hydrology590, 125389.

[9]

Chen, Y.M., Ding, Q.B., Chao, Y.Q., Wei, X.G., Wang, S.Z., Qiu, R.L., 2018. Structural development and assembly patterns of the root-associated microbiomes during phytoremediation. Science of the Total Environment644, 1591–1601.

[10]

Chinese Soil Society, 2000. Agriculture Chemical Analysis of Soil. Beijing: China Agricultural Science and Technology Press.

[11]

Compant, S., Samad, A., Faist, H., Sessitsch, A., 2019. A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. Journal of Advanced Research19, 29–37.

[12]

de Vries, F.T., Griffiths, R.I., Bailey, M., Craig, H., Girlanda, M., Gweon, H.S., Hallin, S., Kaisermann, A., Keith, A.M., Kretzschmar, M., Lemanceau, P., Lumini, E., Mason, K.E., Oliver, A., Ostle, N., Prosser, J.I., Thion, C., Thomson, B., Bardgett, R.D., 2018. Soil bacterial networks are less stable under drought than fungal networks. Nature Communications9, 3033.

[13]

Deng, Y., Jiang, Y.H., Yang, Y.F., He, Z.L., Luo, F., Zhou, J.Z., 2012. Molecular ecological network analyses. BMC Bioinformatics13, 113.

[14]

Dini-Andreote, F., Stegen, J.C., van Elsas, J.D., Van Elsas, J.D., Lladó, S.G., 2015. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Nature Reviews Microbiology13, 789–799.

[15]

Druzhinina, I.S., Seidl-Seiboth, V., Herrera-Estrella, A., Horwitz, B.A., Kenerley, C.M., Monte, E., Mukherjee, P.K., Zeilinger, S., Grigoriev, I.V., Kubicek, C.P., 2011. Trichoderma: the genomics of opportunistic success. Microbiology and Nature Reviews Microbiology9, 749–759.

[16]

Duque-Zapata, J.D., Vélez-Martínez, G.A., Reyes-Ardila, W.L., Florez, J.E.M., López-Álvarez, D., 2025. Seasonal dynamics of soil bacterial and fungal communities in Colombian tropical forests and páramo ecosystems. Soil Ecology Letters7, 250348.

[17]

Egidi, E., Delgado-Baquerizo, M., Plett, J.M., Wang, J.T., Eldridge, D.J., Bardgett, R.D., Maestre, F.T., Singh, B.K., 2019. A few Ascomycota taxa dominate soil fungal communities worldwide. Nature Communications10, 2369.

[18]

Elzinga, C.L., Salzer, D.W., Willoughby, J.W., 2000. Monitoring plant populations: A review of methods and applications. Ecological Applications10, 1251–1269.

[19]

Fakhireh, A., Shoeibi, M., 2025. Autecology of the Euphrates poplar (Populus euphratica Oliv. ) in the Sistan Plain, Iran. Ecopersia13, 153–164.

[20]

Faust, K., Raes, J., 2012. Microbial interactions: from networks to models. Nature Reviews Microbiology10, 538–550.

[21]

Faust, K., Sathirapongsasuti, J.F., Izard, J., Segata, N., Gevers, D., Raes, J., Huttenhower, C., 2012. Microbial co-occurrence relationships in the human microbiome. PLoS Computational Biology8, e1002606.

[22]

Fierer, N., Leff, J.W., Adams, B.J., Nielsen, U.N., Bates, S.T., Lauber, C.L., Owens, S., Gilbert, J.A., Wall, D.H., Caporaso, J.G., 2012. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proceedings of the National Academy of Sciences of the United States of America109, 21390–21395.

[23]

Fierer, N., Wood, S.A., de Mesquita, C.P.B., 2021. How microbes can, and cannot, be used to assess soil health. Soil Biology and Biochemistry153, 108111.

[24]

Gao, Y.Y., Zhang, G.X., Jiang, S.Y., Liu, Y.X., 2024. Wekemo Bioincloud: a user-friendly platform for meta-omics data analyses. iMeta3, e175.

[25]

Hernandez, L.K., Pugliese, G., Ingrisch, J., Fudyma, J., Gil-Loaiza, J., Carpenter, E., Singer, E., Hildebrand, G., Shi, L.L., Hoyt, D.W., Chu, R.K., Toyoda, J., Krechmer, J.E., Claflin, M.S., Ayala-Ortiz, C., Freire-Zapata, V., Pfannerstill, E.Y., Daber, L.E., Meeran, K., Dippold, M.A., Kreuzwieser, J., Williams, J., Ladd, S.N., Werner, C., Tfaily, M.M., Meredith, L.K., 2023. Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest. Nature Microbiology8, 1480–1494.

[26]

Huang, A.C., Jiang, T., Liu, Y.X., Bai, Y.C., Reed, J., Qu, B.Y., Goossens, A., Nützmann, H.W., Bai, Y., Osbourn, A., 2019. A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science364, eaau6389.

[27]

Huang, K.C., Guo, Z.L., Zhao, W., Song, C.G., Wang, H., Li, J.N., Mumin, R., Sun, Y.F., Cui, B.K., 2023. Response of fungal communities to afforestation and its indication for forest restoration. Forest Ecosystems10, 100125.

[28]

Jia, Y.Y., van der Heijden, M.G.A., Wagg, C., Feng, G., Walder, F., 2021. Symbiotic soil fungi enhance resistance and resilience of an experimental grassland to drought and nitrogen deposition. Journal of Ecology109, 3171–3181.

[29]

Jiao, S., Peng, Z.H., Qi, J.J., Gao, J.M., Wei, G.H., 2021. Linking bacterial-fungal relationships to microbial diversity and soil nutrient cycling. mSystems6, e01052–20.

[30]

Kaiser, C., Kilburn, M.R., Clode, P.L., Sletten, J.K., Sanders, I.R., Muhling, R.C., Scully, S.A., Cotton, T.W.P., Bunge, T.C.A., Read, D.J., 2015. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytologist205, 1445–1457.

[31]

Karimi, B., Battle, B., Sébastien, T., Samuel, D., Stéphane, P., Yann, T., Guillaume, N., Alexandre, L., Pierre, P., Jérôme, C., 2020. Biogeography of soil bacteria and archaea across France. Nature Communications11, 3330.

[32]

Kramer, J., Özkaya, Ö., Kümmerli, R., 2020. Bacterial siderophores in community and host interactions. Nature Reviews Microbiology18, 152–163.

[33]

Latifi, H., Nothdurft, A., Koch, B., 2010. Non-parametric prediction and mapping of standing forest volume using TerraSAR-X quadpolarimetric data. Remote Sensing of Environment114, 2237–2247.

[34]

Lewin, A., Murali, G., Rachmilevitch, S., Roll, U., 2024. Global evaluation of current and future threats to drylands and their vertebrate biodiversity. Nature Ecology & Evolution8, 1448–1458.

[35]

Li, J., Wang, X., Zhang, L., Li, Y., Wu, Y., Liu, Q., Zhang, C., Zhang, Y., Qin, S., 2022. Biodiversity decline in the Tarim River Basin. Biological Conservation268, 109501.

[36]

Liu, X., Zhang, G., Li, X., 2023. Standardized soil sampling methods for microbial community analysis in arid ecosystems. Methods in Ecology and Evolution14, 789–801.

[37]

Liu, Y., Zhu, K., Krause, S. M. B., Yang, B., Li, X., Li, C., Huang, W., Chu, H., 2022. Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites. Nature Microbiology7, 1806–1818.

[38]

Liu, Y.Y., Teng, Z.X., Li, Q., Zhou, J.Y., Anwar, E., Yu, C.X., Chen, J., Luo, Z.K., Wang, Y.D., Halik, Ü., Song, Z.L., 2025. Patterns and determinants of plant- and microbial-derived carbon in desert riparian ecosystems: implications for organic C accumulation. CATENA250, 108789.

[39]

Louca, S., Polz, M.F., Mazel, F., Albright, M.B.N., Huber, J.A., O'Connor, M.I., Ackermann, M., Hahn, A.S., Srivastava, D.S., Crowe, S.A., Doebeli, M., Parfrey, L.W., 2018. Function and functional redundancy in microbial systems. Nature Ecology & Evolution2, 936–943.

[40]

Maestre, F.T., Biancari, L., Chen, N., Corrochano-Monsalve, M., Jenerette, G.D., Nelson, C., Shilula, K.N., Shpilkina, Y., 2024. Research needs on the biodiversity–ecosystem functioning relationship in drylands. npj Biodiversity3, 12.

[41]

Martiny, J.B.H., Eisen, J.A., Penn, K., Allison, S.D., Horner-Devine, M.C., 2011. Drivers of bacterial β-diversity depend on spatial scale. Proceedings of the National Academy of Sciences of the United States of America108, 7850–7854.

[42]

Mumin, R., Wang, D.D., Zhao, W., Huang, K.C., Li, J.N., Sun, Y.F., Cui, B.K., 2024. Spatial distribution patterns and assembly processes of abundant and rare fungal communities in Pinus sylvestris var. mongolica forests. Microorganisms12, 977.

[43]

Naylor, D., DeGraaf, S., Purdom, E., Coleman-Derr, D., 2017. Drought and host selection influence bacterial community dynamics in the grass root microbiome. The ISME Journal11, 2691–2704.

[44]

Naylor, D., Sadler, N., Bhattacharjee, A., Graham, E.B., Anderton, C.R., McClure, R., Lipton, M., Hofmockel, K.S., Jansson, J.K., 2020. Soil microbiomes under climate change and implications for carbon cycling. Annual Review of Environment and Resources45, 29–59.

[45]

Neilson, J.W., Califf, K., Cardona, C., Adams, D.C., La Pierre, S.M., Metcalf, S.S., Nowak, A.G., Killian, C.L., Tullis, V.K., Whittaker, C.T., Heintz, K.R., 2017. Significant impacts of increasing aridity on the arid soil microbiome. Applied and Environmental Microbiology83, e00161-17.

[46]

Nielsen, U.N., Ball, B.A., 2015. Impacts of altered precipitation regimes on soil communities and biogeochemistry in arid and semi-arid ecosystems. Global Change Biology21, 1407–1421.

[47]

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., 2020. vegan: Community Ecology Package. R Package Version 2.5–7.

[48]

Paletto, A., Tosi, V., 2009. Forest canopy cover and stand structure in a spruce forest: a comparison of different methods. Journal of Forestry Research20, 151–158.

[49]

Patel, V.K., Kuttippurath, J., Kashyap, R., 2024. Rise in water vapour driven by moisture transport facilitates water availability for the greening of global deserts. Science of the Total Environment946, 174111.

[50]

Payet, R.D., Bilham, L.J., Kabir, S.M.T., Monaco, S., Norcott, A.R., Allen, M.G.E., Zhu, X.Y., Davy, A.J., Brearley, C.A., Todd, J.D., Miller, J.B., 2024. Elucidation of Spartina dimethylsulfoniopropionate synthesis genes enables engineering of stress tolerant plants. Nature Communications15, 8568.

[51]

Peng, L., Wan, Y.B., Li, H., Du, M.D., Shi, Q.D., 2024. Influence of surface water and groundwater gradient on spatial distribution of typical vegetation in the hinterland of Taklamakan desert. Science of the Total Environment953, 176060.

[52]

Sandoval, D.M., Sutton, D.A., Fothergill, A.W., Cano-Lira, J., Gené, J., Decock, C.A., Guarro, J., 2016. Microascus phylogeny and new emerging species. Studies in Mycology83, 193–233.

[53]

Stegen, J.C., Lin, X.J., Fredrickson, J.K., Chen, X.Y., Kennedy, D.W., Murray, C.J., Rockhold, M.L., Konopka, A., 2013. Quantifying community assembly processes and identifying features that impose them. The ISME Journal7, 2069–2079.

[54]

Sun, Y.Z., Li, X.F., Cao, N., Duan, C.X., Ding, C.F., Huang, Y., Wang, J., 2022. Biodegradable microplastics enhance soil microbial network complexity and ecological stochasticity. Journal of Hazardous Materials439, 129610.

[55]

Tayirjiang, A., 2011. Comparative study on vitality dynamics of Populus euphratica Oliv. riparian forests in the lower reaches of Tarim River by ecological water transportation-A case of Arghan. Master Degree Thesis. Xinjiang University, Urumqi, China.

[56]

Tedersoo, L., Mikryukov, V., Anslan, S., Bahram, M., Khalid, A.N., Corrales, A., Agan, A., Vasco-Palacios, A.M., Saitta, A., Antonelli, A., Rinaldi, A.C., Verbeken, A., Sulistyo, B.P., Tamgnoue, B., Furneaux, B., Ritter, C.D., Nyamukondiwa, C., Sharp, C., Marín, C., Dai, D.Q., Gohar, D., Sharmah, D., Biersma, E.M., Cameron, E.K., De Crop, E., Otsing, E., Davydov, E.A., Albornoz, F.E., Brearley, F.Q., Buegger, F., Gates, G., Zahn, G., Bonito, G., Hiiesalu, I., Hiiesalu, I., Zettur, I., Barrio, I.C., Pärn, J., Heilmann-Clausen, J., Ankuda, J., Kupagme, J.Y., Sarapuu, J., Maciá-Vicente, J.G., Fovo, J.D., Geml, J., Alatalo, J.M., Alvarez-Manjarrez, J., Monkai, J., Põldmaa, K., Runnel, K., Adamson, K., Bråthen, K.A., Pritsch, K., Tchan, K.I., Armolaitis, K., Hyde, K.D., Newsham, K.K., Panksep, K., Adebola, L.A., Lamit, L.J., Saba, M., Da Silva Cáceres, M.E., Tuomi, M., Gryzenhout, M., Bauters, M., Bálint, M., Wijayawardene, N., Hagh-Doust, N., Yorou, N.S., Kurina, O., Mortimer, P.E., Meidl, P., Nilsson, R.H., Puusepp, R., Casique-Valdés, R., Drenkhan, R., Garibay-Orijel, R., Godoy, R., Alfarraj, S., Rahimlou, S., Põlme, S., Dudov, S.V., Mundra, S., Ahmed, T., Netherway, T., Henkel, T.W., Roslin, T., Fedosov, V.E., Onipchenko, V.G., Yasanthika, W.A.E., Lim, Y.W., Piepenbring, M., Klavina, D., Kõljalg, U., Abarenkov, K., 2021. The Global Soil Mycobiome consortium dataset for boosting fungal diversity research. Fungal Diversity111, 573–588.

[57]

Tripathi, B.M., Stegen, J.C., Kim, M., Dong, K., Adams, J.M., Lee, Y.K., 2018. Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. The ISME Journal12, 1072–1083.

[58]

Trivedi, P., Leach, J.E., Tringe, S.G., Sa, T., Singh, B.K., 2020. Plant-microbiome interactions: from community assembly to plant health. Nature Reviews Microbiology18, 607–621.

[59]

Tuo, Y., Dong, Z.B., Wang, X.P., Gao, B.B., Zhu, C.M., Tuo, F., 2020. Metagenomics reveal correlations between microbial organisms in soils and the health of populus euphratica. Frontiers in Microbiology11, 2095.

[60]

Van der Heijden, M.G.A., Martin, F.M., Selosse, M.A., Sanders, I.R., 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist205, 1406–1423.

[61]

Wang, D.D., Zhao, W., Reyila, M., Huang, K.C., Liu, S., Cui, B.K., 2022. Diversity of microbial communities of Pinus sylvestris var. mongolica at spatial scale. Microorganisms10, 371.

[62]

Wang, J.T., Zheng, Y.M., Hu, H.W., Zhang, L.M., Li, J., He, J.Z., 2015. Soil pH determines the alpha diversity but not beta diversity of soil fungal community along altitude in a typical Tibetan forest ecosystem. Journal of Soils and Sediments15, 1224–1232.

[63]

Wang, X., Zhang, Y., Li, H., 2023. Dynamics of Populus euphratica forests in arid regions. Ecological Indicators145, 109612.

[64]

Xia, Z., Wang, X., Zhang, Y., 2023. Sex-specific response of rhizosphere microbial communities to drought in Populus euphratica. New Phytologist237, 258–273.

[65]

Yang, J., Feng, Q., Liu, W., 2022a. Crown loss percentage as a robust indicator of Populus euphratica health status in arid environments. Forest Ecology and Management505, 119857.

[66]

Yang, L., Zhang, X., Liu, J., 2022b. Anomalous survival of Populus euphratica in hyper-arid zones. Plant and Soil471, 89–103.

[67]

Yang, P., Zhang, Y., Tariq, M., Liu, X., Yang, G., Luo, S., Lu, Y., Liu, D., Sun, X., 2022c. Plant-microbiome interactions under drought stress: Ecological and physiological perspectives. New Phytologist233, 423–438.

[68]

Zhang, B., Penton, C.R., Xue, C., Qu, Y., Johnson, T.A., Tiedje, J.M., Zhang, Q., 2021. Soil depth and crop determinants of bacterial communities under wheat fields in semiarid agricultural ecosystem. Frontiers in Microbiology12, 610752.

[69]

Zhang, C., Lei, S.L., Wu, H.Y., Liao, L.R., Wang, X.T., Zhang, L., Liu, G.B., Wang, G.L., Fang, L.C., Song, Z.L., 2024. Simplified microbial network reduced microbial structure stability and soil functionality in alpine grassland along a natural aridity gradient. Soil Biology and Biochemistry191, 109366.

[70]

Zhao, W., Huang, K.C., Mumin, R., Li, J.N., Sun, Y.F., Cui, B.K., 2024. Spatial variations impact the soil fungal communities of Larix gmelinii forests in Northeast China. Frontiers in Plant Science15, 1408272.

[71]

Zhou, J.Z., Ning, D.L., 2017. Stochastic community assembly: does it matter in microbial ecology. Microbiology and Molecular Biology Reviews81, e00002-17.

RIGHTS & PERMISSIONS

Higher Education Press

PDF (4586KB)

Supplementary files

Supplementary materials

12

Accesses

0

Citation

Detail

Sections
Recommended

/