Soil amendment strategies determining microbial community composition and their assembly processes in a continuously cropped soil

Hongkai Liao, Chunli Zheng, Juan Li, Jian Long, Yaying Li

PDF(6342 KB)
PDF(6342 KB)
Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (3) : 230219. DOI: 10.1007/s42832-023-0219-x
RESEARCH ARTICLE

Soil amendment strategies determining microbial community composition and their assembly processes in a continuously cropped soil

Author information +
History +

Highlights

● Phyla Proteobacteria and Bacteroidetes dominated in the rhizosphere of tomatoes under RSD amendment.

● Stochastic processes dominated in bacterial community assembly for biochar and CF amendments.

● It is important to monitor and manage soil conditions before planting after RSD amendment.

Abstract

Reductive soil disinfestation (RSD) is an important tool for sustainable agricultural productivity. However, the differences in soil bacterial communities and their community assembly processes among RSD and other treatment strategies (e.g., biochar and chemical fumigation) are still subject to open questions. In this study, soils subjected to various treatments–un-treated control (CK), chemical soil fumigation with CaCN2 (CF), 1% biochar (1%B), 3% biochar (3%B), and reductive soil disinfestation (RSD) are investigated. Soil samples were collected, incubated, and then used for growth of tomato plants. The Sloan neutral community model indicates that stochastic processes dominate in bacterial community assembly for both biochar and CF amendments. In contrast, this work shows that RSD treatment can have a strong impact on soil bacterial community composition. The relative abundance of Firmicutes increased during unplanted soil incubation, whereas Proteobacteria and Bacteroidetes dominated in the rhizosphere after planting of tomatoes. Normalized stochasticity ratio reveals that deterministic selection played an important role in the bacterial assembly under RSD amendment. We found that RSD amendment yielded lower biomass than that for other treatments after 28 days of tomato growth. Our results suggest that although RSD treatment has great potential to rebuild soil bacterial ecology by shaping bacterial communities and their assembly processes, it is important to monitor and manage soil conditions (e.g., soil nutrients or physical properties) before planting to ensure plant productivity.

Graphical abstract

Keywords

amendment strategy / reductive soil disinfestation / bacterial community / assembly processes

Cite this article

Download citation ▾
Hongkai Liao, Chunli Zheng, Juan Li, Jian Long, Yaying Li. Soil amendment strategies determining microbial community composition and their assembly processes in a continuously cropped soil. Soil Ecology Letters, 2024, 6(3): 230219 https://doi.org/10.1007/s42832-023-0219-x

References

[1]
Berthrong, S.T., Yeager, C.M., Gallegos-Graves, L., Steven, B., Eichorst, S.A., Jackson, R.B., Kuske, C.R., 2014. Nitrogen fertilization has a stronger effect on soil nitrogen-fixing bacterial communities than elevated atmospheric CO2. Applied and Environmental Microbiology80, 3103–3112.
CrossRef Google scholar
[2]
Blok, W.J., Lamers, J.G., Termorshuizen, A.J., Bollen, G.J., 2000. Control of soilborne plant pathogens by incorporating fresh organic amendments followed by tarping. Phytopathology90, 253–259.
CrossRef Google scholar
[3]
Bulgarelli, D., Schlaeppi, K., Spaepen, S., Ver Loren van Themaat, E., Schulze-Lefert, P., 2013. Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology64, 807–838.
CrossRef Google scholar
[4]
Butler, D.M., Rosskopf, E.N., Kokalis-Burelle, N., Albano, J.P., Muramoto, J., Shennan, C., 2012. Exploring warm-season cover crops as carbon sources for anaerobic soil disinfestation (ASD). Plant and Soil355, 149–165.
CrossRef Google scholar
[5]
Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods13, 581–583.
CrossRef Google scholar
[6]
Chen, D., Wang, X., Carrión, V.J., Yin, S., Yue, Z., Liao, Y., Dong, Y., Li, X., 2022. Acidic amelioration of soil amendments improves soil health by impacting rhizosphere microbial assemblies. Soil Biology & Biochemistry167, 108599.
CrossRef Google scholar
[7]
Chen, Y., Yang, K., Ye, Y., Zhang, Y., Mi, H., Li, C., Li, Z., Pei, Z., Chen, F., Yan, J., Wang, X., Wang, Y., 2021. Reductive soil disinfestation attenuates antibiotic resistance genes in greenhouse vegetable soils. Journal of Hazardous Materials420, 126632.
CrossRef Google scholar
[8]
Chen, Q.L., Hu, H.W., Yan, Z.Z., Li, C.Y., Nguyen, B.A.T., Sun, A.Q., Zhu, Y.G., He, J.Z., 2021. Deterministic selection dominates microbial community assembly in termite mounds. Soil Biology & Biochemistry152, 108073.
CrossRef Google scholar
[9]
Cuartero, J., Pascual, J.A., Vivo, J.M., Özbolat, O., Sánchez-Navarro, V., Egea-Cortines, M., Zornoza, R., Mena, M.M., Garcia, E., Ros, M., 2022. A first-year melon/cowpea intercropping system improves soil nutrients and changes the soil microbial community. Agriculture, Ecosystems & Environment328, 107856.
CrossRef Google scholar
[10]
Fierer, N., 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nature Reviews Microbiology15, 579–590.
CrossRef Google scholar
[11]
Frenkel, O., Jaiswal, A.K., Elad, Y., Lew, B., Kammann, C., Graber, E.R., 2017. The effect of biochar on plant diseases: what should we learn while designing biochar substrates?. Journal of Environmental Engineering and Landscape Management25, 105–113.
CrossRef Google scholar
[12]
Gkarmiri, K., Mahmood, S., Ekblad, A., Alström, S., Högberg, N., Finlay, R., Loeffler, F.E., 2017. Identifying the active microbiome associated with roots and rhizosphere soil of oilseed rape. Applied and Environmental Microbiology83, e01938–e01917.
CrossRef Google scholar
[13]
Gu, Y., Hou, Y., Huang, D., Hao, Z., Wang, X., Wei, Z., Jousset, A., Tan, S., Xu, D., Shen, Q., Xu, Y., Friman, V.P., 2017. Application of biochar reduces Ralstonia solanacearum infection via effects on pathogen chemotaxis, swarming motility, and root exudate adsorption. Plant and Soil415, 269–281.
CrossRef Google scholar
[14]
Guo, H., Zhao, X., Rosskopf, E.N., Di Gioia, F., Hong, J.C., McNear, D.H. Jr, 2018. Impacts of anaerobic soil disinfestation and chemical fumigation on soil microbial communities in field tomato production system. Applied Soil Ecology126, 165–173.
CrossRef Google scholar
[15]
Huang, X., Liu, L., Wen, T., Zhang, J., Wang, F., Cai, Z., 2016. Changes in the soil microbial community after reductive soil disinfestation and cucumber seedling cultivation. Applied Microbiology and Biotechnology100, 5581–5593.
CrossRef Google scholar
[16]
Huang, X., Liu, L., Zhao, J., Zhang, J., Cai, Z., 2019b. The families Ruminococcaceae, Lachnospiraceae, and Clostridiaceae are the dominant bacterial groups during reductive soil disinfestation with incorporated plant residues. Applied Soil Ecology135, 65–72.
CrossRef Google scholar
[17]
Huang, X., Zhao, J., Zhou, X., Zhang, J., Cai, Z., 2019a. Differential responses of soil bacterial community and functional diversity to reductive soil disinfestation and chemical soil disinfestation. Geoderma348, 124–134.
CrossRef Google scholar
[18]
Jaiswal, A.K., Elad, Y., Graber, E.R., Frenkel, O., 2014. Rhizoctonia solani suppression and plant growth promotion in cucumber as affected by biochar pyrolysis temperature, feedstock and concentration. Soil Biology & Biochemistry69, 110–118.
CrossRef Google scholar
[19]
Jaiswal, A.K., Elad, Y., Paudel, I., Graber, E.R., Cytryn, E., Frenkel, O., 2017. Linking the belowground microbial composition, diversity and activity to soilborne disease suppression and growth promotion of tomato amended with biochar. Scientific Reports7, 1–17.
CrossRef Google scholar
[20]
Jiang, Y., Kang, Y., Han, C., Zhu, T., Deng, H., Xie, Z., Zhong, W., 2020. Biochar amendment in reductive soil disinfestation process improved remediation effect and reduced N2O emission in a nitrate-riched degraded soil. Archives of Agronomy and Soil Science66, 983–991.
CrossRef Google scholar
[21]
Jien, S.H., Wang, C.S., 2013. Effects of biochar on soil properties and erosion potential in a highly weathered soil. Catena110, 225–233.
CrossRef Google scholar
[22]
Kolton, M., Meller Harel, Y., Pasternak, Z., Graber, E.R., Elad, Y., Cytryn, E., 2011. Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants. Applied and Environmental Microbiology77, 4924–4930.
CrossRef Google scholar
[23]
Liao, H., Chapman, S.J., Li, Y., Yao, H.Y., 2018. Dynamics of microbial biomass and community composition after short-term water status change in Chinese paddy soils. Environmental Science and Pollution Research International25, 2932–2941.
CrossRef Google scholar
[24]
Liao, H., Fan, H., Li, Y., Yao, H., 2021a. Influence of reductive soil disinfestation or biochar amendment on bacterial communities and their utilization of plant-derived carbon in the rhizosphere of tomato. Applied Microbiology and Biotechnology105, 815–825.
CrossRef Google scholar
[25]
Liao, H., Li, Y., Yao, H., 2019. Biochar amendment stimulates utilization of plant-derived carbon by soil bacteria in an intercropping system. Frontiers in Microbiology10, 1361.
CrossRef Google scholar
[26]
Liao, H., Zheng, C., Long, J., Guzmán, I., 2021b. Effects of biochar amendment on tomato rhizosphere bacterial communities and their utilization of plant-derived carbon in a calcareous soil. Geoderma396, 115082.
CrossRef Google scholar
[27]
Lidbury, I.D., Borsetto, C., Murphy, A.R., Bottrill, A., Jones, A.M., Bending, G.D., Hammond, J.P., Chen, Y., Wellington, E.M., Scanlan, D.J., 2021. Niche-adaptation in plant-associated Bacteroidetes favours specialisation in organic phosphorus mineralisation. ISME Journal15, 1040–1055.
CrossRef Google scholar
[28]
Love, M.I., Huber, W., Anders, S., 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology15, 550.
CrossRef Google scholar
[29]
McMurdie, P.J., Holmes, S., 2013. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One8, e61217.
CrossRef Google scholar
[30]
Ning, D., Deng, Y., Tiedje, J.M., Zhou, J., 2019. A general framework for quantitatively assessing ecological stochasticity. Proceedings of the National Academy of Sciences of the United States of America116, 16892–16898.
CrossRef Google scholar
[31]
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’hara, R., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2013. Package ‘vegan’. Community ecology package, version2, 1–295.
[32]
Olsen, S.R., 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture
[33]
Orr, R., Nelson, P.N., 2018. Impacts of soil abiotic attributes on Fusarium wilt, focusing on bananas. Applied Soil Ecology132, 20–33.
CrossRef Google scholar
[34]
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., 2012. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research41, D590–D596.
CrossRef Google scholar
[35]
Shakoor, A., Shahzad, S.M., Chatterjee, N., Arif, M.S., Farooq, T.H., Altaf, M.M., Tufail, M.A., Dar, A.A., Mehmood, T., 2021. Nitrous oxide emission from agricultural soils: Application of animal manure or biochar? A global meta-analysis.. Journal of Environmental Management285, 112170.
CrossRef Google scholar
[36]
Sloan, W.T., Lunn, M., Woodcock, S., Head, I.M., Nee, S., Curtis, T.P., 2006. Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environmental Microbiology8, 732–740.
CrossRef Google scholar
[37]
Stopnisek, N., Shade, A., 2021. Persistent microbiome members in the common bean rhizosphere: an integrated analysis of space, time, and plant genotype. ISME Journal15, 2708–2722.
CrossRef Google scholar
[38]
Team, R.C., 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2012
[39]
Uematsu, S., Tanaka-Miwa, C., Sato, R., Kobara, Y., Sato, M., 2007. Ethyl alcohol as a promising material of reductive soil disinfestation for controlling root knot nematode and soilborne plant diseases, Proc. 2007 Ann. Inter. Res. Conf. Methyl Bromide Alternatives and Emissions Reductions, pp. 75.71–75.73
[40]
Ulbrich, T.C., Rivas-Ubach, A., Tiemann, L.K., Friesen, M.L., Evans, S.E., 2022. Plant root exudates and rhizosphere bacterial communities shift with neighbor context. Soil Biology & Biochemistry172, 108753.
CrossRef Google scholar
[41]
van Agtmaal, M., van Os, G., Hol, G., Hundscheid, M., Runia, W., Hordijk, C., De Boer, W., 2015. Legacy effects of anaerobic soil disinfestation on soil bacterial community composition and production of pathogen-suppressing volatiles. Frontiers in Microbiology6, 6.
CrossRef Google scholar
[42]
Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry19, 703–707.
CrossRef Google scholar
[43]
Yan, Y., Wu, R., Li, S., Su, Z., Shao, Q., Cai, Z., Huang, X., Liu, L., 2022. Reductive soil disinfestation enhances microbial network complexity and function in intensively cropped greenhouse soil. Horticulturae8, 476.
CrossRef Google scholar
[44]
Zhang, H., Zheng, X., Wang, X., Xiang, W., Xiao, M., Wang, L., Zhang, Y., Song, K., Zhao, Z., Lv, W., Chen, J., Ge, T., 2022. Effect of fertilization regimes on continuous cropping growth constraints in watermelon is associated with abundance of key ecological clusters in the rhizosphere. Agriculture, Ecosystems & Environment339, 108135.
CrossRef Google scholar
[45]
Zhao, J., Liu, S., Zhou, X., Xia, Q., Liu, X., Zhang, S., Zhang, J., Cai, Z., Huang, X., 2020. Reductive soil disinfestation incorporated with organic residue combination significantly improves soil microbial activity and functional diversity than sole residue incorporation. Applied Microbiology and Biotechnology104, 7573–7588.
CrossRef Google scholar
[46]
Zhu, W., Wang, W., Hong, C., Ding, J., Zhu, F., Hong, L., Yao, Y., 2022. Influence of reductive soil disinfestation on the chemical and microbial characteristics of a greenhouse soil infested with Fusarium oxysporum. Physiological and Molecular Plant Pathology118, 101805.
CrossRef Google scholar
[47]
Zimmerman, A.R., 2010. Abiotic and microbial oxidation of laboratory-produced black carbon (biochar). Environmental Science & Technology44, 1295–1301.
CrossRef Google scholar

Acknowledgments

This work was funded by the National Natural Science Foundation of China (42167017), Talents of Guizhou Science and Technology Cooperation Platform ([2017]5726-52), Guizhou Province 100-level Talent Project ([2020]6010), the Key Program of Science and Technology of Guizhou Province ([2020]1Z036), and Ningbo Municipal Science and Technology Bureau ([2021]Z047).

Authors’ contribution

YL, HL and CZ conceived the experiment. JL and YL finished incubation and analyzed samples to collect data, analyzed and visualized data. HL and YL wrote the draft. YL reviewed the manuscript and all the authors made significant contributions in result presentation. YL and CZ provided funding, project administration and supervision.

Data availability

Main data generated or analyzed during this study are included in this manuscript and supplementary material. Extra data supporting the findings of this study are available from the corresponding author upon reasonable request.

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-023-0219-x and is accessible for authorized users.

RIGHTS & PERMISSIONS

2023 Higher Education Press
AI Summary AI Mindmap
PDF(6342 KB)

Accesses

Citations

Detail

Sections
Recommended

/