Articles | Volume 22, issue 16
https://doi.org/10.5194/bg-22-4221-2025
© Author(s) 2025. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-22-4221-2025
© Author(s) 2025. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
26 Aug 2025
Research article |
| 26 Aug 2025
| 26 Aug 2025
Soil microbial diversity and network complexity promote phosphorus transformation – a case of long-term mixed plantations of Eucalyptus and a nitrogen-fixing tree species
Jiyin Li
Guangxi Key Laboratory of Forest Ecology and Conservation, Guangxi Colleges and Universities Key Laboratory for Cultivation and Utilization of Subtropical Forest Plantation, College of Forestry, Guangxi University, Nanning, Guangxi 530004, China
Yeming You
Guangxi Key Laboratory of Forest Ecology and Conservation, Guangxi Colleges and Universities Key Laboratory for Cultivation and Utilization of Subtropical Forest Plantation, College of Forestry, Guangxi University, Nanning, Guangxi 530004, China
Guangxi Youyiguan Forest Ecosystem National Observation and Research Station, Youyiguan Forest Ecosystem Observation and Research Station of Guangxi, Pingxiang, Guangxi 532600, China
Wen Zhang
Jinggangshan Institute of Red Soil, Jiangxi Academy of Agricultural Sciences, Ji'an Jiangxi 343016, China
Yi Wang
Institute of Resources and Environment, Key Laboratory of National Forestry and Grassland Administration/Beijing for Bamboo & Rattan Science and Technology, International Centre for Bamboo and Rattan, Beijing 100102, China
Yuying Liang
Guangxi Key Laboratory of Forest Ecology and Conservation, Guangxi Colleges and Universities Key Laboratory for Cultivation and Utilization of Subtropical Forest Plantation, College of Forestry, Guangxi University, Nanning, Guangxi 530004, China
Haimei Huang
Guangxi Key Laboratory of Forest Ecology and Conservation, Guangxi Colleges and Universities Key Laboratory for Cultivation and Utilization of Subtropical Forest Plantation, College of Forestry, Guangxi University, Nanning, Guangxi 530004, China
Hailun Ma
Guangxi Key Laboratory of Forest Ecology and Conservation, Guangxi Colleges and Universities Key Laboratory for Cultivation and Utilization of Subtropical Forest Plantation, College of Forestry, Guangxi University, Nanning, Guangxi 530004, China
Qinxia He
Guangxi Key Laboratory of Forest Ecology and Conservation, Guangxi Colleges and Universities Key Laboratory for Cultivation and Utilization of Subtropical Forest Plantation, College of Forestry, Guangxi University, Nanning, Guangxi 530004, China
Angang Ming
Guangxi Youyiguan Forest Ecosystem National Observation and Research Station, Youyiguan Forest Ecosystem Observation and Research Station of Guangxi, Pingxiang, Guangxi 532600, China
Experimental Centre of Tropical Forestry, Chinese Academy of Forestry, Pingxiang 532600, China
Guangxi Key Laboratory of Forest Ecology and Conservation, Guangxi Colleges and Universities Key Laboratory for Cultivation and Utilization of Subtropical Forest Plantation, College of Forestry, Guangxi University, Nanning, Guangxi 530004, China
Guangxi Youyiguan Forest Ecosystem National Observation and Research Station, Youyiguan Forest Ecosystem Observation and Research Station of Guangxi, Pingxiang, Guangxi 532600, China
Cited articles
Adams, R. I., Miletto, M., Taylor, J. W., and Bruns, T. D.: Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances, ISME J., 7, 1262–1273, https://doi.org/10.1038/ismej.2013.28, 2013.
Banerjee, S., Schlaeppi, K., and van der Heijden, M. G.: Keystone taxa as drivers of microbiome structure and functioning, Nat. Rev. Microbiol, 16, 567–576, https://doi.org/10.1038/s41579-018-0024-1, 2018.
Benjamini, Y., Krieger, A. M., and Yekutieli, D.: Adaptive linear step-up procedures that control the false discovery rate, Biometrika, 93, 491–507, https://doi.org/10.1093/biomet/93.3.491, 2006.
Bünemann, E. K., Smernik, R. J., Marschner, P., McNeill, A. M.: Microbial synthesis of organic and condensed forms of phosphorus in acid and calcareous soils, Soil Biol. Biochem., 40, 932–946, https://doi.org/10.1016/j.soilbio.2007.11.012, 2008.
Burns, R. C. and Hardy, R. W.: Nitrogen fixation in bacteria and higher plants, Springer Science & Business Media 21:192, 2012.
Cao, N., Zhi, M., Zhao, W., Pang, J., Hu, W., Zhou, Z., and Meng, Y.: Straw retention combined with phosphorus fertilizer promotes soil phosphorus availability by enhancing soil P-related enzymes and the abundance of phoC and phoD genes, Soil Till. Res., 220, 105390, https://doi.org/10.1016/j.still.2022.105390, 2022.
Cheng, J., Zhao, M., Cong, J., Qi, Q., Xiao, Y., Cong, W., Deng, Y., Zhou, J., and Zhang, Y.: Soil pH exerts stronger impacts than vegetation type and plant diversity on soil bacterial community composition in subtropical broad-leaved forests, Plant Soil, 450, 273–286, https://doi.org/10.1007/s11104-020-04507-2, 2020.
Chen, S., Lin, L., Deng, Y., Yuan, S., and Zhang, N.: Tree species richness and mycorrhizal types drive soil nitrogen cycling by regulating soil microbial community composition and diversity in tropical forests, Forest Ecol. Manag., 569, 122187, https://doi.org/10.1016/j.foreco.2024.122187, 2024.
Cornell, C. R., Zhang, Y., Ning, D., Xiao, N., Wagle, P., Xiao, X., and Zhou, J.: Land use conversion increases network complexity and stability of soil microbial communities in a temperate grassland, ISME J., 17, 2210–2220, https://doi.org/10.1038/s41396-023-01521-x, 2023.
Dai, Z., Liu, G., Chen, H., Chen, C., Wang, J., Ai, S., Wei, D., Li, D. Ma, B., Tang, C., Brookes, P. C., and Xu, J.: Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems, ISME J., 14, 757–770, https://doi.org/10.1038/s41396-019-0567-9, 2020.
Pereira, A. P. A., Andrade, P. A. M., de Andrade, P. A. M., Bini, D., Durrer, A., Robin, A., Bouillet, J. P., Andreote, F. D., and Cardoso, E. J. B. N.: Shifts in the bacterial community composition along deep soil profiles in monospecific and mixed stands of Eucalyptus grandis and Acacia mangium, PloS one, 12, e0180371, https://doi.org/10.1371/journal.pone.0180371, 2017.
Delgado-Baquerizo, M., Reich, P. B., Khachane, A. N., Campbell, C. D., Thomas, N., Freitag, T. E., Al-Soud, W. A., Sørensen, S., Bardgett, R. D., and Singh, B. K.: It is elemental: soil nutrient stoichiometry drives bacterial diversity, Environ. Microbiol., 19, 1176–1188, https://doi.org/10.1111/1462-2920.13642, 2017.
Delmas, E., Besson, M., Brice, M. H., Burkle, L. A., Dalla Riva, G. V., Fortin, M. J., Gravel, D., Guimarães, P. R., Guimarães Jr., P. R., Hembry, D. H., Newman, E. A., Olesen, J. M., Pires, M. M., Yeakel, J. D., and Poisot, T.: Analysing ecological networks of species interactions, Biol. Rev., 94, 16–36, https://doi.org/10.1111/brv.12433, 2019.
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., and Bardgett, R. D.: Soil bacterial networks are less stable under drought than fungal networks, Nat. Commun., 9, 3033, https://doi.org/10.1038/s41467-018-05516-7, 2018.
Dong, H., Ge, J., Sun, K., Wang, B., Xue, J., Wakelin, S. A., Wu, J., Sheng, W., Xu, Q., Jiang, P., Chen, J., and Qin, H.: Change in root-associated fungal communities affects soil enzymatic activities during Pinus massoniana forest development in subtropical China, Forest Ecol. Manag., 482, 118817, https://doi.org/10.1016/j.foreco.2020.118817, 2021.
Du, E., Terrer, C., Pellegrini, A. F., Ahlström, A., van Lissa, C. J., Zhao, X., X, N., Wu, X., and Jackson, R. B.: Global patterns of terrestrial nitrogen and phosphorus limitation, Nat. Geosci., 13, 221–226, https://doi.org/10.1038/s41561-019-0530-4, 2020.
Egidi, E., Delgado-Baquerizo, M., Plett, J. M., Wang, J., Eldridge, D. J., Bardgett, R. D., Maestre, F. T., and Singh, B. K.: A few Ascomycota taxa dominate soil fungal communities worldwide, Nat. Commun., 10, 2369, https://doi.org/10.1038/s41467-019-10373-z, 2019.
Epron, D., Nouvellon, Y., Mareschal, L., e Moreira, R. M., Koutika, L. S., Geneste, B., Delgado-Rojas, J, S., Laclau J, P., Sola, G., Gonçalves, J, L, M., and Bouillet, J. P.: Partitioning of net primary production in Eucalyptus and Acacia stands and in mixed-species plantations: two case-studies in contrasting tropical environments, Forest Ecol. Manag., 301, 102–111, https://doi.org/10.1016/j.foreco.2012.10.034, 2013.
Fan, K., Weisenhorn, P., Gilbert, J. A., and Chu, H.: Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil, Soil Biol. and Biochem., 125, 251–260, https://doi.org/10.1016/j.soilbio.2018.07.022, 2018.
Fan, Y., Zhong, X., Lin, F., Liu, C., Yang, L., Wang, M., Chen, G., Chen, Y., and Yang, Y.: Responses of soil phosphorus fractions after nitrogen addition in a subtropical forest ecosystem: Insights from decreased Fe and Al oxides and increased plant roots, Geoderma, 337, 246–255, https://doi.org/10.1016/j.geoderma.2018.09.028, 2019.
Faust, K.: Open challenges for microbial network construction and analysis, ISME J., 15, 3111–3118, https://doi.org/10.1038/s41396-021-01027-4, 2021.
Fraser, T., Lynch, D. H., Entz, M. H., and Dunfield, K. E.: Linking alkaline phosphatase activity with bacterial phoD gene abundance in soil from a long-term management trial, Geoderma, 257, 115–122, https://doi.org/10.1016/j.geoderma.2014.10.016, 2015.
Fu, L., Yan, Y., Li, X., Liu, Y., and Lu, X.: Rhizosphere soil microbial community and its response to different utilization patterns in the semi-arid alpine grassland of northern Tibet, Front. Microbiol, 13, 931795, https://doi.org/10.3389/fmicb.2022.931795, 2022.
Gao, C., Xu, L., Montoya, L., Madera, M., Hollingsworth, J., Chen, L., Purdom, E., Singan, V., Vogel, J., Hutmacher, R. B., Dahlberg, J. A., Coleman-Derr, D., Lemaux, P. G., and Taylor, J. W.: Co-occurrence networks reveal more complexity than community composition in resistance and resilience of microbial communities, Nat. Commun., 13, 3867, https://doi.org/10.1038/s41467-022-31343-y, 2022.
Graham, E. B., Knelman, J. E., Schindlbacher, A., Siciliano, S., Breulmann, M., Yannarell, A., Beman, J. M., Abell, G., Philippot, L., Prosser, J., Foulquier1, A., Yuste, J. C., Glanville, H. C., Jones, D. L., Angel, R., Salminen, J., Newton, R. J., Bürgmann, H., Ingram, L. J., Hamer, U., Siljanen, H. M. P., Peltoniemi, K., Potthast, K., Bañeras, L., Hartmann, M., Banerjee, S., Yu, R. Q., Nogaro, G., Richter, A., Koranda, M., Castle, S. C., Goberna, M., Song, B., Chatterjee, A., Nunes, O. C., Lopes, A. R., Cao, Y., Kaisermann, A., Hallin, S., Strickland, M. S., Garcia-Pausas, J., Barba, J., Kang, H., Isobe, K., Papaspyrou, S., Pastorelli, R., Lagomarsino, A., Lindström, E. S., Basiliko, N., and Nemergut1, D. R.: Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?, Front. Microbial, 7, 214, https://doi.org/10.3389/fmicb.2016.00214, 2016.
Guo, Q. and Gong, L.: Compared with pure forest, mixed forest alters microbial diversity and increases the complexity of interdomain networks in arid areas, Microbiology Spectrum, 12, e02642-23, https://doi.org/10.1128/spectrum.02642-23, 2024.
Guo, Y., Hou, L., Zhang, Z., Zhang, J., Cheng, J., Wei, G., and Lin, Y.: Soil microbial diversity during 30 years of grassland restoration on the Loess Plateau, China: Tight linkages with plant diversity, Land Degrad. Dev., 30, 1172–1182, https://doi.org/10.1002/ldr.3300, 2019.
Guo, Y., Xu, T., Cheng, J., Wei, G., and Lin, Y.: Above-and belowground biodiversity drives soil multifunctionality along a long-term grassland restoration chronosequence, Sci. Total Environ., 772, 145010, https://doi.org/10.1016/j.scitotenv.2021.145010, 2021.
He, Y., Wen Y., Li, K., Ye, S., Zhang, H., He, F., Fan, R., and Wu, H.: Responses of soil multifunctionality, microbial diversity, and network complexity to tree species mixing in Eucalyptus plantations, Ind. Crop. Prod., 225, 120575, https://doi.org/10.1016/j.indcrop.2025.120575, 2025.
Hinsinger, P.: Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review, Plant Soil, 237, 173–195, https://doi.org/10.1023/A:1013351617532, 2001.
Hu, J. P., Zhang, M. X., Lü, Z. L., He, Y. Y., Yang, X. X., Khan, A., Xiong, Y. C., Fang, X. L., Dong, Q. M., and Zhang, J. L.: Grazing practices affect phyllosphere and rhizosphere bacterial communities of Kobresia humilis by altering their network stability, Sci. Total Environ., 900, 165814, https://doi.org/10.1016/j.scitotenv.2023.165814, 2023.
Hu, Y., Xia, Y., Sun, Q. I., Liu, K., Chen, X., Ge, T., Zhu, B., Zhu, Z., Zhang, Z., Su, Y.: Effects of long-term fertilization on phoD-harboring bacterial community in Karst soils, Sci. Total Environ., 628, 53–63, https://doi.org/10.1016/j.scitotenv.2018.01.314, 2018.
Huang, X., Liu, S., Wang, H., Hu, Z., Li, Z., and You, Y.: Changes of soil microbial biomass carbon and community composition through mixing nitrogen-fixing species with Eucalyptus urophylla in subtropical China, Soil Biol. Biochem., 73, 42–48, https://doi.org/10.1016/j.soilbio.2014.01.021, 2014.
Huang, X., Liu, S., You, Y., Wen, Y., Wang, H., and Wang, J.: Microbial community and associated enzymes activity influence soil carbon chemical composition in Eucalyptus urophylla plantation with mixing N2-fixing species in subtropical China, Plant Soil, 414, 199–212, https://doi.org/10.1007/s11104-016-3117-5, 2017.
Jiao, S., Yang, Y., Xu, Y., Zhang, J., and Lu, Y.: Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China, ISME J., 14, 202–216, https://doi.org/10.1038/s41396-019-0522-9, 2020.
Jin, X., Liu, Y., Hu, W., Wang, G., Kong, Z., Wu, L., and Ge, G.: Soil bacterial and fungal communities and the associated nutrient cycling responses to forest conversion after selective logging in a subtropical forest of China, Forest Ecol. Manag., 444, 308–317, https://doi.org/10.1016/j.foreco.2019.04.032, 2019.
Kang, L., Zhang, G., and Chu, G.: Split delivering phosphorus via fertigation to a calcareous soil increased P availability and maize yield (Zea mays L.) by reducing P fixation, J. Soil. Sediment., 21, 2287–2300, https://doi.org/10.1007/s11368-021-02914-1, 2021.
Khan, A., Zhang, G., Li, T., and He, B.: Fertilization and cultivation management promotes soil phosphorus availability by enhancing soil P-cycling enzymes and the phosphatase encoding genes in bulk and rhizosphere soil of a maize crop in sloping cropland, Ecotox. Environ., Safe, 264, 115441, https://doi.org/10.1016/j.ecoenv.2023.115441, 2023.
Knowles, S. C. L., Eccles, R. M., and Baltrūnaitė, L.: Species identity dominates over environment in shaping the microbiota of small mammals, Ecol. Lett., 22, 826–837, https://doi.org/10.1111/ele.13240, 2019.
Koutika, L. S. and Mareschal, L.: Acacia and eucalypt change P, N and C concentrations in POM of Arenosols in the Congolese coastal plains, Geoderma Reg., 11, 37–43, https://doi.org/10.1016/j.geodrs.2017.07.009, 2017.
Koutika, L. S. and Richardson, D. M.: Acacia mangium Willd: benefits and threats associated with its increasing use around the world, For. Ecosyst., 6, 2, https://doi.org/10.1186/s40663-019-0159-1, 2019.
Lang, F., Bauhus, J., Frossard, E., George, E., Kaiser, K., Kaupenjohann, M., Krüger, J., Matzner, E., Polle, A., Prietzel, J., Rennenberg, H., and Wellbrock, N.: Phosphorus in forest ecosystems: new insights from an ecosystem nutrition perspective, J. Plant Nutr. Soil Sc., 179, 129–135, https://doi.org/10.1002/jpln.201500541, 2016.
Li, J. and Huang, X.: Data set for “Soil microbial diversity and network complexity promote phosphorus transformation – a case of long-term mixed plantations of Eucalyptus and a nitrogen-fixing tree species”, in: Biogeosciences, Guangxi University, Zenodo [data set], https://doi.org/10.5281/zenodo.16901157, 2025.
Li, C., Xu, Y., Wang, Z., Zhu, W., and Du, A.: Mixing planting with native tree species reshapes soil fungal community diversity and structure in multi-generational eucalypt plantations in southern China, Front. Microbiol. Fro., 14, 1132875, https://doi.org/10.3389/fmicb.2023.1132875, 2023.
Li, M., You, Y., Tan, X., Wen, Y., Yu, S., Xiao, N., Shen, W., and Huang, X.: Mixture of N2-fixing tree species promotes Po accumulation and transformation in topsoil aggregates in a degraded karst region of subtropical China, Geoderma, 413, 115752, https://doi.org/10.1016/j.geoderma.2022.115752, 2022.
Li, N., Zhang, Y., Qu, Z., Liu, B., Huang, L., Ming, A., and Sun, H.: Mixed and continuous cropping eucalyptus plantation facilitated soil carbon cycling and fungal community diversity after a 14-year field trail, Ind. Crop. Prod., 210, 118157, https://doi.org/10.1016/j.indcrop.2024.118157, 2024.
Li, Q., Lv, J., Peng, C., Xiang, W., Xiao, W., and Song, X.: Nitrogen-addition accelerates phosphorus cycling and changes phosphorus use strategy in a subtropical Moso bamboo forest, Environ. Res. Lett., 16, 024023, https://doi.org/10.1088/1748-9326/abd5e1, 2021.
Li, Y., Niu, S., and Yu, G.: Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: A meta-analysis, Glob. Change Biol., 22, 934-943, https://doi.org/10.1111/gcb.13125, 2016.
Liu, S., Yu, H., Yu, Y., Huang, J., Zhou, Z., Zeng, J., Chen, P., Xiao, F., He, Z., and Yan, Q.: Ecological stability of microbial communities in Lake Donghu regulated by keystone taxa, Ecol. Indic., 136, 108695, https://doi.org/10.1016/j.ecolind.2022.108695, 2022.
Liu, S., Li, H., Xie, X., Chen, Y., Lang, M., and Chen, X.: Long-term moderate fertilization increases the complexity of soil microbial community and promotes regulation of phosphorus cycling genes to improve the availability of phosphorus in acid soil, Appl. Soil Ecol., 194, 105178, https://doi.org/10.1016/j.apsoil.2023.105178, 2024.
Lu, X., Wen, L., Sun, H., Fei, T., Liu, H., Ha, S., Tang, S., and Wang, L.: Responses of soil respiration to phosphorus addition in global grasslands: A meta-analysis, J. Clean. Prod., 349, 131413, https://doi.org/10.1016/j.jclepro.2022.131413, 2022.
Luo, G., Sun, B., Li, L., Li, M., Liu, M., Zhu, Y., Guo, S., Ling, N., and Shen, Q.: Understanding how long-term organic amendments increase soil phosphatase activities: insight into phoD-and phoC-harboring functional microbial populations, Soil Biol. Biochem., 139, 107632, https://doi.org/10.1016/j.soilbio.2019.107632, 2019.
Ma, B., Wang, Y., Ye, S., Liu, S., Stirling, E., Gilbert, J. A., Faust, K., Knight, R., Jansson, J. K., Cardona, C., Röttjers, L., and Xu, J.: Earth microbial co-occurrence network reveals interconnection pattern across microbiomes, Microbiome, 8, 82, https://doi.org/10.1186/s40168-020-00857-2, 2020.
Meyer, J. B., Frapolli, M., Keel, C., and Maurhofer, M.: Pyrroloquinoline quinone biosynthesis gene pqqC, a novel molecular marker for studying the phylogeny and diversity of phosphate-solubilizing pseudomonads, Appl. Environ. Microb., 77, 7345–7354, https://doi.org/10.1128/AEM.05434-11, 2011.
Ming, L. I., Ming, L. I. U., Li, Z. P., Jiang, C. Y., and Meng, W. U.: Soil N transformation and microbial community structure as affected by adding biochar to a paddy soil of subtropical China, J. Integr. Agr., 15, 209–219, https://doi.org/10.1016/S2095-3119(15)61136-4, 2016.
Monecke, A. and Leisch, F.: semPLS: structural equation modeling using partial least squares, J. Stat. Softw., 48, 1–32, https://doi.org/10.18637/jss.v048.i03, 2012.
Mori, H., Maruyama, F., Kato, H., Toyoda, A., Dozono, A., Ohtsubo, Y., Nagata, Y., Fujiyama, A., Tsuda, M., and Kurokawa, K.: Design and experimental application of a novel non-degenerate universal primer set that amplifies prokaryotic 16S rRNA genes with a low possibility to amplify eukaryotic rRNA genes, DNA Res., 21, 217–227, https://doi.org/10.1093/dnares/dst052, 2014.
Murphy, J. and Riley, J. P.: A modified single solution method for the determination of phosphate in natural waters, Anal. Chim. Acta, 27, 31–36, https://doi.org/10.1016/S0003-2670(00)88444-5, 1962.
Nannipieri, P., Giagnoni, L., Renella, G., Puglisi, E., Ceccanti, B., Masciandaro, G., Fornasier, F., Moscatelli, M. C., and Marinari, S.: Soil enzymology: classical and molecular approaches, Biol. Fert. Soil., 48, 743–762, https://doi.org/10.1007/s00374-012-0723-0, 2012.
Niraula, S.: Effects of a N2-Fixing Biofertilizer on the Rhizosphere Microbiome and the Influence of Biochar on Soil Fertility and Microbial Communities, The University of Texas at Arlington, 2021.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'hara, R. B., Solymos, P., Stevens, M. H. H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., Caceres, M. D., Durand, S., Evangelista, H. B. A., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M. O., Lahti, L., McGlinn, D., Ouellette, M. H., Cunha, E. R., Smith, T., Stier, A., Braak, C. J. K. T., and Weedon, J.: Package “vegan”, Community ecology package, version, 2, 1–295, https://github.com/vegandevs/vegan (last access: 29 April 2025), 2013.
Parada, A. E., Needham, D. M., and Fuhrman, J. A.: Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples, Environ. Microbiol., 18, 1403–1414, https://doi.org/10.1111/1462-2920.13023, 2016.
Pastore, G., Kaiser, K., Kernchen, S., and Spohn, M.: Microbial release of apatite-and goethite-bound phosphate in acidic forest soils, Geoderma, 370, 114360, https://doi.org/10.1016/j.geoderma.2020.114360, 2020.
Paula, R. R., Bouillet, J. P., Trivelin, P. C. O., Zeller, B., de Moraes Gonçalves, J. L., Nouvellon, Y., Bouvet, J, M., Plassard, C., and Laclau, J. P.: Evidence of short-term belowground transfer of nitrogen from Acacia mangium to Eucalyptus grandis trees in a tropical planted forest, Soil Biol. Biochem., 91, 99–108, https://doi.org/10.1016/j.soilbio.2015.08.017, 2015.
Peng, Y., Duan, Y., Huo, W., Xu, M., Yang, X., Wang, X., Wang, B., Blackwell, M. S. A., and Feng, G.: Soil microbial biomass phosphorus can serve as an index to reflect soil phosphorus fertility, Biol. Fert. Soils, 57, 657–669, https://doi.org/10.1007/s00374-021-01559-z, 2021.
Pereira, A. P. A., Durrer, A., Gumiere, T., Gonçalves, J. L. M., Robin, A., Bouillet, J. P., Wang, J., Verma, J. P., Singh, B. K., and Cardoso, E. J. B. N.: Mixed Eucalyptus plantations induce changes in microbial communities and increase biological functions in the soil and litter layers, Forest Ecol. Manag., 433, 332–342, https://doi.org/10.1016/j.foreco.2018.11.018, 2019.
Philippot, L., Chenu, C., Kappler, A., Rillig, M. C., and Fierer, N.: The interplay between microbial communities and soil properties, Nat. Rev. Microbiol., 22, 226–239, https://doi.org/10.1038/s41579-023-00980-5, 2024.
Poudel, R., Jumpponen, A., Schlatter, D. C., Paulitz, T. C., Gardener, B. M., Kinkel, L. L., and Garrett, K. A.: Microbiome networks: a systems framework for identifying candidate microbial assemblages for disease management, Phytopathology, 106, 1083–1096, https://doi.org/10.1094/PHYTO-02-16-0058-FI, 2016.
Qiao, Y., Wang, T., Huang, Q., Guo, H., Zhang, H., Xu, Q., Shen, Q., and Ling, N.: Core species impact plant health by enhancing soil microbial cooperation and network complexity during community coalescence, Soil Biol. Biochem., 188, 109231, https://doi.org/10.1016/j.soilbio.2023.109231, 2024.
Qin, F., Yang, F., Ming, A., Jia, H., Zhou, B., Xiong, J., and Lu, J.: Mixture enhances microbial network complexity of soil carbon, nitrogen and phosphorus cycling in Eucalyptus plantations, Forest Ecol. Manag., 553, 121632, https://doi.org/10.1016/j.foreco.2023.121632, 2024.
Qiu, L., Zhang, Q., Zhu, H., Reich, P. B., Banerjee, S., van der Heijden, M. G., Sadowsky, M. J., Ishii, S., Jia, X., Shao, M., Liu, B., Jiao, H., Li, H., and Wei, X.: Erosion reduces soil microbial diversity, network complexity and multifunctionality, ISME J., 15, 2474–2489, https://doi.org/10.1038/s41396-021-00913-1, 2021.
Rachid, C. T., Balieiro, F. D. C., Peixoto, R. S., Pinheiro, Y. A. S., Piccolo, M. D. C., Chaer, G. M., and Rosado, A. S.: Mixed plantations can promote microbial integration and soil nitrate increases with changes in the N cycling genes, Soil Biol. Biochem., 66, 146–153, https://doi.org/10.1016/j.soilbio.2013.07.005, 2013.
Ragot, S. A., Kertesz, M. A., and Bünemann, E. K.: phoD alkaline phosphatase gene diversity in soil, Appl. Environ. Microb., 81, 7281–7289, https://doi.org/10.1128/AEM.01823-15, 2015.
Sanchez, G.: PLS path modeling with R. Berkeley: Trowchez Editions, http://www.gastonsanchez.com/PLS (last access: 7 October 2024) Path Modeling with R.pdf, 2013.
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Horn, D. J. V., and Weber, C. F.: Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities, Appl. Environ. Microb., 75, 7537–7541, https://doi.org/10.1128/AEM.01541-09, 2009.
See, C. R., Yanai, R. D., Fisk, M. C., Vadeboncoeur, M. A., Quintero, B. A., and Fahey, T. J.: Soil nitrogen affects phosphorus recycling: foliar resorption and plant–soil feedbacks in a northern hardwood forest, Ecology, 96, 2488–2498, https://doi.org/10.1890/15-0188.1, 2015.
Shi, Y., Delgado Baquerizo, M., Li, Y., Yang, Y., Zhu, Y. G., Peñuelas, J., and Chu, H.: Abundance of kinless hubs within soil microbial networks are associated with high functional potential in agricultural ecosystems, Environ. Int., 142, 105869, https://doi.org/10.1016/j.envint.2020.105869, 2020.
Siciliano, S. D., Palmer, A. S., Winsley, T., Lamb, E., Bissett, A., Brown, M. V., van Dorst, J., Ji, M., Ferrari, B. C., Grogan, P., Chu, H., and Snape, I.: Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities, Soil Biol. Biochem., 78, 10–20, https://doi.org/10.1016/j.soilbio.2014.07.005, 2014.
Soltangheisi, A., Withers, P. J., Pavinato, P. S., Cherubin, M. R., Rossetto, R., Do Carmo, J. B., da Rocha, G., C., and Martinelli, L. A.: Improving phosphorus sustainability of sugarcane production in Brazil, GCB Bioenergy, 11, 1444–1455, https://doi.org/10.1111/gcbb.12650, 2019.
Soumare, A., Diedhiou, A. G., Thuita, M., Hafidi, M., Ouhdouch, Y., Gopalakrishnan, S., and Kouisni, L.: Exploiting biological nitrogen fixation: a route towards a sustainable agriculture, Plants, 9, 1011, https://doi.org/10.3390/plants9081011, 2020.
Sprent, J. I. and Platzmann, J.: Nodulation in legumes, Kew: Royal Botanic Gardens, 2001.
Stougaard, J.: Regulators and regulation of legume root nodule development, Plant Physiol., 124, 531–540, https://doi.org/10.1104/pp.124.2.531, 2000.
Sun, H., Wu, Y., Zhou, J., Yu, D., and Chen, Y.: Microorganisms drive stabilization and accumulation of organic phosphorus: An incubation experiment, Soil Biol. Biochem., 172, 108750, https://doi.org/10.1016/j.soilbio.2022.108750, 2022.
Tan, H., Barret, M., Mooij, M. J., Rice, O., Morrissey, J. P., Dobson, A., Griffiths, B., and O'Gara, F.: Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils, Biol. Fert. Soils, 49, 661–672, https://doi.org/10.1007/s00374-012-0755-5, 2013.
Tchichelle, S. V., Epron, D., Mialoundama, F., Koutika, L. S., Harmand, J. M., Bouillet, J. P., and Mareschal, L.: Differences in nitrogen cycling and soil mineralisation between a eucalypt plantation and a mixed eucalypt and Acacia mangium plantation on a sandy tropical soil, South, Forests, 79, 1–8, https://doi.org/10.2989/20702620.2016.1221702, 2017.
Tenenhaus, M., Amato, S., and Esposito Vinzi, V.: A global goodness-of-fit index for PLS structural equation modeling. In Proceedings of the XLII SIS Scientific Meeting, 739–742, Padova, CLEUP, https://www.researchgate.net/publication/284462849 (last accesds: 7 October 2024), 2004.
Tian, J., Ge, F., Zhang, D., Deng, S., and Liu, X.: Roles of phosphate solubilizing microorganisms from managing soil phosphorus deficiency to mediating biogeochemical P cycle, Biology, 10, 158, https://doi.org/10.3390/biology10020158, 2021.
Tsiknia, M., Tzanakakis, V. A., Oikonomidis, D., Paranychianakis, N. V., and Nikolaidis, N. P.: Effects of olive mill wastewater on soil carbon and nitrogen cycling, Appl. Microbiol. Biot., 98, 2739–2749, https://doi.org/10.1007/s00253-013-5272-4, 2014.
Turner, B., Brenes Arguedas, T., and Condit, R.: Pervasive phosphorus limitation of tree species but not communities in tropical forests, Nature, 555, 367–370, https://doi.org/10.1038/nature25789, 2018.
Waithaisong, K., Robin, A., l'Huillery, V., Abadie, J., Sauvage, F. X., Chemardin, P., Mareschal, L., Bouillet, J.-P., Gonçalves, J. L. M., and Plassard, C.: Organic phosphorus immobilization in microbial biomass controls how N2-fixing trees affect phosphorus bioavailability in two tropical soils, Environmental Advances, 8, 100247, https://doi.org/10.1016/j.envadv.2022.100247, 2022.
Wang, Q., Wang, J., Li, Y., Chen, D., Ao, J., Zhou, W., Shen, D., Li, Q., Huang, Z., and Jiang, Y.: Influence of nitrogen and phosphorus additions on N2-fixation activity, abundance, and composition of diazotrophic communities in a Chinese fir plantation, Sci. Total Environ., 619, 1530–1537, https://doi.org/10.1016/j.scitotenv.2017.10.064, 2018.
Wang, Y., Luo, D., Xiong, Z., Wang, Z., and Gao, M.: Changes in rhizosphere phosphorus fractions and phosphate-mineralizing microbial populations in acid soil as influenced by organic acid exudation, Soil Till. Res., 225, 105543, https://doi.org/10.1016/j.still.2022.105543, 2023.
Widdig, M., Heintz-Buschart, A., Schleuss, P. M., Guhr, A., Borer, E. T., Seabloom, E. W., and Spohn, M.: Effects of nitrogen and phosphorus addition on microbial community composition and element cycling in a grassland soil, Soil Biol. Biochem, 151, 108041, https://doi.org/10.1016/j.soilbio.2020.108041, 2020.
Yan, J., Huang, X., Su, X., Zhang, W., Gao, G., and You, Y.: Introducing N2-Fixing Tree Species into Eucalyptus Plantation in Subtropical China Alleviated Carbon and Nitrogen Constraints within Soil Aggregates, Forests, 13, 2102, https://doi.org/10.3390/f13122102, 2022.
Yang, J., Lan, L., Jin, Y., Yu, N., Wang, D., and Wang, E.: Mechanisms underlying legume–rhizobium symbioses, J. Integr. Plant Biol., 64, 244–267, https://doi.org/10.1111/jipb.13207, 2022.
Yao, X., Zhang, Q., Zhou, H., Zhu, H., Nong, Z., Ye, S., and Deng, Q.: Introduction of Dalbergia odorifera enhances nitrogen absorption on Eucalyptus through stimulating microbially mediated soil nitrogen-cycling, For. Ecosyst., 8, 59, https://doi.org/10.1186/s40663-021-00339-3, 2021.
Yao, X., Hui, D., Xing, S., Zhang, Q., Chen, J., Li, Z., Xu, Y., and Deng, Y.: Mixed plantations with N-fixing tree species maintain ecosystem
Yu, Q., Ma, S., Ni, X., Ni, X., Guo, Z., Tan, X., Zhong, M., Hanif, MA., Zhu, J., Ji, C., and Zhu, B.: Long-term phosphorus addition inhibits phosphorus transformations involved in soil arbuscular mycorrhizal fungi and acid phosphatase in two tropical rainforests, Geoderma, 425, 116076, https://doi.org/10.1016/j.geoderma.2022.116076, 2022.
Yuan, M. M., Guo, X., Wu, L., Zhang, Y. A., Xiao, N., Ning, D., Shi, Z., Zhou, X., Wu, L., Yang, Y., Tiedje, J. M., and Zhou, J.: Climate warming enhances microbial network complexity and stability, Nat. Clim. Change, 11, 343–348, https://doi.org/10.1038/s41558-021-00989-9, 2021.
Yuste, J. C., Penuelas, J., Estiarte, M., Garcia-Mas, J., Mattana, S., Ogaya, R., Pujol, M., and Sardans, J.: Drought-resistant fungi control soil organic matter decomposition and its response to temperature, Glob. Change Biol., 17, 1475–1486, https://doi.org/10.1111/j.1365-2486.2010.02300.x, 2011.
Zeng, Q., Peñuelas, J., Sardans, J., Zhang, Q., Zhou, J., Yue, K., Chen, C., Yang, Y., and Fan, Y.: Keystone bacterial functional module activates P-mineralizing genes to enhance enzymatic hydrolysis of organic P in a subtropical forest soil with 5-year N addition, Soil Biol. Biochem., 192, 109383, https://doi.org/10.1016/j.soilbio.2024.109383, 2024.
Zhang, M., O'Connor, P. J., Zhang, J., and Ye, X.: Linking soil nutrient cycling and microbial community with vegetation cover in riparian zone, Geoderma, 384, 114801, https://doi.org/10.1016/j.geoderma.2020.114801, 2021.
Zhang, W., You, Y., Su, X., Yan, J., Gao, G., Ming, A., Shen, W., and Huang, X.: Introducing N2-fixing tree species into Eucalyptus plantations promotes soil organic carbon sequestration in aggregates by increasing microbial carbon use efficiency, Catena, 231, 107321, https://doi.org/10.1016/j.catena.2023.107321, 2023.
Zhang, Y. and Wang, X.: Geographical spatial distribution and productivity dynamic change of eucalyptus plantations in China, Sci. Rep.-UK, 11, 19764, https://doi.org/10.1038/s41598-021-97089-7, 2021.
Zhou, Y., Boutton, T. W., and Wu, X. B.: Soil phosphorus does not keep pace with soil carbon and nitrogen accumulation following woody encroachment, Glob. Change Biol., 24, 1992–2007, https://doi.org/10.1111/gcb.14048, 2018.
Short summary
We introduced nitrogen-fixing tree species into Eucalyptus plantations. The results showed that nitrogen-fixing tree species mixed plantations increased microbial diversity and network complexity, as well as the abundance of genes related to the nitrogen and phosphorus cycles, while promoting soil phosphorus transformation. This suggests that mixed plantings could be a promising forest management strategy for enhancing phosphorus use efficiency in ecosystems.
We introduced nitrogen-fixing tree species into Eucalyptus plantations. The results showed that...
Altmetrics
Final-revised paper
Preprint