Abstract
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Organic fertilization increased the richness and abundance of beneficial communities.
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The increase in the beneficial communities resulted from soil property optimization.
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Organic fertilization enhanced the functionality of bacterial communities.
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Plants exhibited a preference for internalizing beneficial bacteria.
Soil microbiomes play a crucial role in maintaining ecological functions and are of great importance for soil health. Some of them could bring benefits to plants for growth promotion. Despite numerous studies have focused on specific beneficial bacteria and their interactions with soils and plants, we still lack a comprehensive understanding of beneficial communities in plant-soil continuums and their responses to agricultural activities. To address this gap, we carried out a microcosm experiment using 16S rRNA amplicon sequencing to explore the effects of organic fertilization on beneficial communities in plant–soil continuums and assess their potential multifunctionality. Our findings reveal that organic fertilization had a positive impact on the beneficial functionality of bacterial communities in plant-soil continuums. This improvement was primarily attributed to the optimized soil physicochemical conditions resulting from organic fertilization. Additionally, organic fertilization increased the complexity of bacterial co-occurrence networks in both soils and the endosphere. Keystone taxa in the endosphere undergone a shift of functions toward pathogen suppression as the result of organic fertilization. Furthermore, this study revealed that plants exhibited a preference for internalizing beneficial bacteria over other type of bacteria. We also provided new insights for evaluating the multifunctionality of microbiomes, and found that the functionality of beneficial communities in plant-soil continuums is enhanced by organic fertilization. All these findings suggested that organic fertilization can be an effective strategy for maintaining plant and soil health.
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Adeleke, B.S., Babalola, O.O., 2021. Roles of plant endosphere microbes in agriculture-a review. Journal of Plant Growth Regulation 41, 1411–1422.
Bresson, J., Varoquaux, F., Bontpart, T., Touraine, B., Vile, D., 2013. The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytologist 200, 552–569.
Caetano-Anollés, G., Crist-Estes, D.K., Bauer, W.D., 1922. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. Journal of Bacteriology 170, 3164–3169.
Chen, D., Wang, X., Zhang, W., Zhou, Z., Ding, C., Liao, Y., Li, X., 2020a. Persistent organic fertilization reinforces soil-borne disease suppressiveness of rhizosphere bacterial community. Plant and Soil 452, 313–322.
Chen, H., Li, W., Zheng, W., Yin, C., Fan, X., Ye, M., Gao, Z., Wu, C., Liang, Y., 2023a. Linking nitrogen- and straw-sensitive indicator species and their co-occurrences to priming effect in agricultural soil exposed to long-term nitrogen fertilization. Soil Biology & Biochemistry 176, 102221.
Chen, L., Chen, S., Zhang, Y., Long, Y., Kong, X., Wang, S., Li, L., Wang, F., Sun, Y., Xu, A., 2023b. Co-occurrence network of microbial communities affected by application of anaerobic fermentation residues during phytoremediation of ionic rare earth tailings area. Science of the Total Environment 856, 159223.
Chen, Q.L., Ding, J., Zhu, D., Hu, H.W., Delgado-Baquerizo, M., Ma, Y.B., He, J.Z., Zhu, Y.G., 2020b. Rare microbial taxa as the major drivers of ecosystem multifunctionality in long-term fertilized soils. Soil Biology & Biochemistry 141, 107626.
Chen, S., Waghmode, T.R., Sun, R., Kuramae, E.E., Hu, C., Liu, B., 2019. Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome 7, 136.
Compant, S., Clément, C., Sessitsch, A., 2010. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biology & Biochemistry 42, 669–672.
Compant, S., Reiter, B., Sessitsch, A., Nowak, J., Clement, C., Ait Barka, E., 2005. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Applied and Environmental Microbiology 71, 1625–1693.
Dai, X.L., Song, D.L., Guo, Q.K., Zhou, W., Liu, G.R., Ma, R.P., Liang, G.Q., He, P., Sun, G., Yuan, F.S., Liu, Z.B., 2021. Predicting the influence of fertilization regimes on potential N fixation through their effect on free-living diazotrophic community structure in double rice cropping systems. Soil Biology & Biochemistry 156, 102220.
Del Valle, I., Webster, T.M., Cheng, H.Y., Thies, J.E., Kessler, A., Miller, M.K., Ball, Z.T., Mackenzie, K.R., Masiello, C.A., Silberg, J.J., Lehmann, J., 2020. Soil organic matter attenuates the efficacy of flavonoid-based plant-microbe communication. Science Advances 6, eaax2254.
Deng, X.H., Zhang, N., Li, Y.C., Zhu, C.Z., Qu, B.Y., Liu, H.J., Li, R., Bai, Y., Shen, Q.R., Salles, J.F., 2022. Bio-organic soil amendment promotes the suppression of Ralstonia solanacearum by inducing changes in the functionality and composition of rhizosphere bacterial communities. New Phytologist 235, 1552–1574.
Dong, M., Zhao, M., Shen, Z., Deng, X., Ou, Y., Tao, C., Liu, H., Li, R., Shen, Q., 2020. Biofertilizer application triggered microbial assembly in microaggregates associated with tomato bacterial wilt suppression. Biology and Fertility of Soils 56, 551–563.
Dowling, D.N., O’Gara, F., 1994. Metabolites of Pseudomonas involved in the biocontrol of plant disease. Trends in Biotechnology 12, 133–141.
Hartmann, M., Six, J., 2022. Soil structure and microbiome functions in agroecosystems. Nature Reviews Earth & Environment 4, 4–12.
Housh, A.B., Powell, G., Scott, S., Anstaett, A., Gerheart, A., Benoit, M., Waller, S., Powell, A., Guthrie, J.M., Higgins, B., Wilder, S.L., Schueller, M.J., Ferrieri, R.A., 2021. Functional mutants of Azospirillum brasilense elicit beneficial physiological and metabolic responses in Zea mays contributing to increased host iron assimilation. ISME Journal 15, 1505–1522.
Kwak, M.J., Kong, H.G., Choi, K., Kwon, S.K., Song, J.Y., Lee, J., Lee, P.A., Choi, S.Y., Seo, M., Lee, H.J., Jung, E.J., Park, H., Roy, N., Kim, H., Lee, M.M., Rubin, E.M., Lee, S.W., Kim, J.F., 2012. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nature Biotechnology 36, 1100–1109.
Lehmann, J., Bossio, D.A., Kogel-Knabner, I., Rillig, M.C., 2020. The concept and future prospects of soil health. Nature Reviews Earth & Environment 1, 544–553.
Li, H., La, S., Zhang, X., Gao, L., Tian, Y., 2021. Salt-induced recruitment of specific root-associated bacterial consortium capable of enhancing plant adaptability to salt stress. ISME Journal 15, 2265–2222.
Li, W.J., Li, H.Z., An, X.L., Lin, C.S., Li, L.J., Zhu, Y.G., 2022. Effects of manure fertilization on human pathogens in endosphere of three vegetable plants. Environmental Pollution 314, 120344.
Liu, H., Li, J., Carvalhais, L.C., Percy, C.D., Prakash Verma, J., Schenk, P.M., Singh, B.K., 2021. Evidence for the plant recruitment of beneficial microbes to suppress soil-borne pathogens. New Phytologist 229, 2273–2225.
Luo, J., Liao, G., Banerjee, S., Gu, S., Liang, J., Guo, X., Zhao, H., Liang, Y., Li, T., 2023. Long-term organic fertilization promotes the resilience of soil multifunctionality driven by bacterial communities. Soil Biology & Biochemistry 177, 102922.
Mendes, L.W., Mendes, R., Raaijmakers, J.M., Tsai, S.M., 2012. Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean. ISME Journal 12, 3032–3042.
Mendes, R., Kruijt, M., de Bruijn, I., Dekkers, E., van der Voort, M., Schneider, J.H., Piceno, Y.M., DeSantis, T.Z., Andersen, G.L., Bakker, P.A., Raaijmakers, J.M., 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100.
Okazaki, S., Kaneko, T., Sato, S., Saeki, K., 2013. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proceedings of the National Academy of Sciences of the United States of America 110, 17131–17136.
Ren, A.Z., Li, X., Han, R., Yin, L.J., Wei, M.Y., Gao, Y.B., 2011. Benefits of a symbiotic association with endophytic fungi are subject to water and nutrient availability in Achnatherum sibiricum. Plant and Soil 346, 363–373.
Rivas, R., Velazquez, E., Willems, A., Vizcaino, N., Subba-Rao, N. S., Mateos, P.F., Gillis, M., Dazzo, F.B., Martinez-Molina, E., 2002. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L. f.) druce. Applied and Environmental Microbiology 68, 5217–5222.
Rudrappa, T., Czymmek, K.J., Pare, P.W., Bais, H.P., 2002. Rootsecreted malic acid recruits beneficial soil bacteria. Plant Physiology 148, 1547–1556.
Santoyo, G., Orozco-Mosqueda, M.C., Govindappa, M., 2012. Mechanisms of biocontrol and plant growth-promoting activity in soil bacterial species of Bacillus and Pseudomonas: a review. Biocontrol Science and Technology 22, 255–272.
Sasse, J., Martinoia, E., Northen, T., 2012. Feed your friends: Do plant exudates shape the root microbiome? Trends in Plant Science 23, 25–41.
Shi, S., Nuccio, E.E., Shi, Z.J., He, Z., Zhou, J., Firestone, M.K., 2016. The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages. Ecology Letters 19, 926–936.
Sun, A.Q., Jiao, X.Y., Chen, Q.L., Wu, A.L., Zheng, Y., Lin, Y.X., He, J.Z., Hu, H.W., 2021a. Microbial communities in crop phyllosphere and root endosphere are more resistant than soil microbiota to fertilization. Soil Biology & Biochemistry 153, 108113.
Sun, R., Wang, F., Hu, C., Liu, B., 2021b. Metagenomics reveals taxon-specific responses of the nitrogen-cycling microbial community to long-term nitrogen fertilization. Soil Biology & Biochemistry 156, 108214.
Sun, S., Ma, B., Wang, G., Tan, X., 2023. Linking microbial biogeochemical cycling genes to the rhizosphere of pioneering plants in a glacier foreland. Science of the Total Environment 872, 161944.
Toro, M., Azcon, R., Barea, J.M., 1998. The use of isotopic dilution techniques to evaluate the interactive effects of Rhizobium genotype, mycorrhizal fungi, phosphate-solubilizing rhizobacteria and rock phosphate on nitrogen and phosphorus acquisition by Medicago sativa. New Phytologist 138, 265–273.
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 Microbiology 18, 607–621.
Vives-Peris, V., de Ollas, C., Gomez-Cadenas, A., Perez-Clemente, R.M., 2020. Root exudates: from plant to rhizosphere and beyond. Plant Cell Reports 39, 3–17.
Vorholt, J.A., 2012. Microbial life in the phyllosphere. Nature Reviews Microbiology 10, 828–840.
Wei, Z., Yang, T., Friman, V.P., Xu, Y., Shen, Q., Jousset, A., 2015. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nature Communications 6, 8413.
Xiong, C., He, J.Z., Singh, B.K., Zhu, Y.G., Wang, J.T., Li, P.P., Zhang, Q.B., Han, L.L., Shen, J.P., Ge, A.H., Wu, C.F., Zhang, L. M., 2021a. Rare taxa maintain the stability of crop mycobiomes and ecosystem functions. Environmental Microbiology 23, 1907–1924.
Xiong, C., Zhu, Y.G., Wang, J.T., Singh, B., Han, L.L., Shen, J.P., Li, P.P., Wang, G.B., Wu, C.F., Ge, A.H., Zhang, L.M., He, J.Z., 2021b. Host selection shapes crop microbiome assembly and network complexity. New Phytologist 229, 1091–1104.
Yu, P., He, X., Baer, M., Beirinckx, S., Tian, T., Moya, Y.A.T., Zhang, X., Deichmann, M., Frey, F.P., Bresgen, V., Li, C., Razavi, B.S., Schaaf, G., von Wiren, N., Su, Z., Bucher, M., Tsuda, K., Goormachtig, S., Chen, X., Hochholdinger, F., 2021. Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nature Plants 7, 481–499.
Zhang, L., Zhang, M., Huang, S., Li, L., Gao, Q., Wang, Y., Zhang, S., Huang, S., Yuan, L., Wen, Y., Liu, K., Yu, X., Li, D., Zhang, L., Xu, X., Wei, H., He, P., Zhou, W., Philippot, L., Ai, C., 2022a. A highly conserved core bacterial microbiota with nitrogen-fixation capacity inhabits the xylem sap in maize plants. Nature Communications 13, 3361.
Zhang, L., Zhang, W., Li, Q., Cui, R., Wang, Z., Wang, Y., Zhang, Y. Z., Ding, W., Shen, X., 2020. Deciphering the root endosphere microbiome of the desert plant Alhagi sparsifolia for drought resistance-promoting bacteria. Applied and Environmental Microbiology 86, e02863–19.
Zhang, S.T., Liu, X.J., Zhou, L.H., Deng, L.Y., Zhao, W.Z., Liu, Y., Ding, W., 2022b. Alleviating soil acidification could increase disease suppression of bacterial wilt by recruiting potentially beneficial rhizobacteria. Microbiology Spectrum 10, e0233321.
Zhang, Y.J., Hu, H.W., Chen, Q.L., Singh, B.K., Yan, H., Chen, D., He, J.Z., 2019. Transfer of antibiotic resistance from manureamended soils to vegetable microbiomes. Environment International 130, 104912.
Zhao, Z.B., He, J.Z., Geisen, S., Han, L.L., Wang, J.T., Shen, J.P., Wei, W.X., Fang, Y.T., Li, P.P., Zhang, L.M., 2019. Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. Microbiome 7, 33.
Zhou, J., Deng, Y., Luo, F., He, Z., Yang, Y., Relman, D., 2011. Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio 2, e00122–11.
Acknowledgments
We thank Prof. Yong-Guan Zhu for valuable comments and suggestions to improve the quality of this manuscript. This work was financially supported by the State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products (No.2021DG700024-KF202307).
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Enhancement of Beneficial Microbiomes in Plant-Soil Continuums through Organic Fertilization: Insights into the Composition and Multifunctionality
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Li, WJ., Zhou, XY., An, XL. et al. Enhancement of beneficial microbiomes in plant–soil continuums through organic fertilization: Insights into the composition and multifunctionality. Soil Ecol. Lett. 6, 230223 (2024). https://doi.org/10.1007/s42832-023-0223-1
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DOI: https://doi.org/10.1007/s42832-023-0223-1