Study on soil microbial interaction with nutrients under different shelterbelts in Baiquan County

Abstract

As an essential base for agricultural products in Baiquan County China, the black soil inthe Northeast region had soil nutrient contentsup to several times that of ordinary soil. However, over-exploitation and utilization in recent years led to a decline in the quality of black soil. Therefore, it is strategic significance to study the improvement of soil quality by different shelterbelts. In order to explore the interaction between soil microbial and nutrients, the soils under four shelterbelts (pure Pinus sylvestris forest, pure Larix gmelinii forest, mixed Pinus sylvestris forest and mixed Larix gmelinii forest) were used as the research materials in Baiquan County, Heilongjiang Province, China. The changes of soil physicochemical properties and soil microbial function genes were studied, and their interaction patterns were analyzed by Redundancy analysis (RDA). The results showed that the concentration changes of TOC (total organic carbon), TN (total nitrogen), {\text{NO}}_{\text{3}}^{-}-N (nitrate nitrogen concentration), {\text{NH}}_{\text{4}}^{+}-N (ammonium nitrogen), TP (total phosphorus) and SP (soil available phosphorus) were significantly (P < 0.05) increased in rhizosphere soil under mixed Larix gmelinii forest. In non-rhizosphere soil, the concentration changes of TOC, TN, {\text{NO}}_{\text{3}}^{-}-N and AN (soil alkali hydrolyzed nitrogen) were significantly (P < 0.05) increased under mixed Larix gmelinii forest. In a word, the concentration changes of TOC, TN, {\text{NO}}_{\text{3}}^{-}-N were significantly (P < 0.05) increased in soil under mixed Larix gmelinii forest. In cropland soil, the concentration changes of {\text{NO}}_{\text{3}}^{-}-N, {\text{NH}}_{\text{4}}^{+}-N, TP and SP were significantly (P < 0.05) increased besides pure Pinus sylvestris forest. The abundance analysis of soil function genes revealed that amoA-AOA, nifH, nirS, nosZ, narG and phoD were upregulated under the mixed Larix gmelinii forest. The changes in abundance of amoA-AOA and nirS played an important role in increasing soil nutrient concentration and promoting the utilization of soil nutrients. The study suggested the cropland soil quality was improved by the mixed Larix gmelinii forest, it should provide clear evidence for importance of the microbial-abundance in the soil nutrients improvement.

Graphical abstract

Keywords

shelterbelts / soil nutrients / soil microbial function genes abundance / Baiquan County

Highlight

	● Shelter forests in the agricultural field can increase forest productivity, improve soil fertility and achieve better ecological benefits.
	● The amoA and nirS genes, which played vital roles in the changes of soil nutrients concentration indiced that Larix gmelinii forest was used as the most suitable shelter forests to enhance soil nutrients, which accelerated soil nutrients cyclic utilization.
	● It provided a clear evidence for importance of the microbial-abundance in the soil N cycle sequestration.

References

[1] Ahmed, W., Huang, J., Liu, K., Qaswar, M., Khan, M.N., Chen, J., Sun, G., Huang, Q.H., Liu, Y.R., Liu, G.G., Sun, M., Li, C., Li, D.C., Ali, S., Normatov, Y., Mehmood, S., Zhang, H.M., 2019. Changes in phosphorus fractions associated with soil chemical properties under long-term organic and inorganic fertilization in paddy soils of southern China. PLoS One10, e0216881.

[2] Awasthi, P., Bargali, K., Bargali, S.S., Jhariya, M.K., 2022a. Structure and functioning of Coriaria nepalensis dominated shrublands in degraded hills of Kumaun Himalaya. I. Dry matter dynamics. Land Degradation & Development33, 1474–1494.

[3] Awasthi, P., Bargali, K., Bargali, S.S., Khatri, K., Jhariya, M.K., 2022b. Nutrient partitioning and dynamics in Coriaria nepalensis wall dominated shrublands of degraded hills of kumaun Himalaya. Frontiers in Forests and Global Change5, 913127.

[4] Baptistella, J.L.C., de Andrade, S.A.L., Favarin, J.L., Mazzafera, P., 2020. Urochloa in tropical agroecosystems. Frontiers in Sustainable Food Systems4, 119.

[5] Barros, F.M.D.R., Fracetto, F.J.C., Lira Junior, M.A., Bertini, S.C.B., Fracetto, G.G.M., 2021. Spatial and seasonal responses of diazotrophs and ammonium-oxidizing bacteria to legume-based silvopastoral systems. Applied Soil Ecolog158, 103797.

[6] Chen, X.P., Yang, J.N., Zhu, X.E., Liang, X., Lei, Y.R., He, C.Q., 2016. N-fixing trees in wetland restoration plantings: effects on nitrogensupply and soil microbial communities. Environmental Science and Pollution Research23, 24749–24757.

[7] Cheng, W., Parton, W.J., Gonzalez-Meler, M.A., Phillips, R., Asao, S., McNickle, G.G., Brzostek, E., Jastrow, J.D., 2014. Synthesis and modeling perspectives of rhizosphere priming. New Phytologist201, 31–44.

[8] Cheng, Y., Elrys, A.S., Merwad, A.R.M., Zhang, H.M., Chen, Z.X., Zhang, J.B., Cai, Z.C., Müller, C., 2022. Global patterns and drivers of soil dissimilatory nitrate reduction to ammonium. Environmental Science & Technology56, 3791–3800.

[9] Daebeler, A., Kitzinger, K., Koch, H., Herbold, C.W., Steinfeder, M., Schwarz, J., Zechmeister, T., Karst, S.M., Albertsen, M., Nielsen, P.H., 2020. Exploring the upper pH limits of nitrite oxidation: diversity, ecophysiology, and adaptive traits of haloalkalitolerant Nitrospira. ISME Journal14, 2967–2979.

[10] Ding, K., Zhong, L., Xin, X.P., Xu, Z.H., Kang, X.M., Liu, W.J., Rui, Y.C., Jiang, L.L., Tang,L ., Wang, Y.F., 2015. Effect of grazing on the abundance of functional genes associated with N cycling in three types of grassland in Inner Mongolia. Journal of Soils and Sediments15, 683–693.

[11] Feng, Y.H., Schmid, B., Loreau, M., Forrester, D.I., Fei, S.L., Zhu, JX., Tang, Z.Y., Zhu, J.L., Hong, P.B., Ji, C.J., Shi, Y., Su, H.J., Xiong, X.Y., Xiao, J., Wang, S.P., Fang, J.Y., 2022. Multispecies forest plantations outyield monocultures across a broad range of conditions. Science376, 865–868.

[12] Fierer, N., Jackson, R.B., 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America103, 626–631.

[13] Finzi, A.C., Abramoff, R.Z., Spiller, K.S., Brzostek, E.R., Darby, B.A., Kramer, M.A., Phillips, R.P., 2015. Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Global Change Biology21, 2082–2094.

[14] Fraser, T.D., Lynch, D.H., Gaiero, J., Khosla, K., Dunfield, K.E., 2017. Quantification of bacterial non-specific acid (phoC) and alkaline (phoD) phosphatase genes in bulk and rhizosphere soil from organically managed soybean fields. Applied Soil Ecology111, 48–56.

[15] Gubry-Rangin, C., Kratsch, C., Williams, T.A., McHardy, A.C., Embley, T.M., Prosser, J.I., Macqueen, D.J., 2015. Coupling of diversification and pH adaptation during the evolution of terrestrial thaumarchaeota. Proceedings of the National Academy of Sciences of the United States of America112, 9370–9375.

[16] Gutiérrez Castorena, E.V., del Carmen Gutiérrez-Castorena, M., Vargas, T.G., Bontemps, L.C., Martínez, J.D., Méndez, E.S., Solorio, C.A.O., 2016. Micromapping of microbial hotspots and biofilms from different crops using digital image mosaics of soil thin sections. Geoderma279, 11–21.

[17] Hao, C.L., Xiao, W.H., Zhou, Y.Y., Wang, Y., 2019. Phosphorus balance in typical rainfield of black soil region in Northeast China. Geosciences Journal23, 637–648.

[18] Hao, J.Q., Feng, Y.Z., Wang, X., Yu, Q., Zhang, F., Yang, G.H., Ren, G.X., Han, X.H., Wang, X.J., Ren, C.J., 2022. Soil microbial nitrogen-cycling gene abundances in response to crop diversification: a meta-analysis. Science of the Total Environment838, 156621.

[19] Hu, H.W., Chen, D., He, J.Z., 2015. Microbial regulation of terrestrial nitrous oxide formation: Understanding the biological pathways for prediction of emission rates. FEMS Microbiology Reviews39, 729–749.

[20] Kalam, S., Basu, A., Ahmad, I., Sayyed, R.Z., El-Enshasy, H.A., Dailin, D.J., Suriani, N.L., 2020. Recent understanding of soil acidobacteria and their ecological significance: a critical review. Frontiers in Microbiology11, 580024–580024.

[21] Kupka, D., Gruba, P., 2022. Effect of pH on the sorption of dissolved organic carbon derived from six tree species in forest soils. Ecological Indicators140, 108975.

[22] Lang, M., Li, P., Ti, C.P., Zhu, S.X., Yan, X.Y., Chang, S.X., 2019. Soil gross nitrogen transformations are related to land-uses in two agroforestry systems. Ecological Engineering127, 431–439.

[23] Levy-Booth, D.J., Prescott, C.E., Grayston, S.J., 2014. Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biology and Biochemistry75, 11–25.

[24] Li, D., Liu, C.M., Luo, R., Sadakane, K., Lam, T.W., 2015. MEGAHIT: an ultra-fast single node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics31, 1674–1676.

[25] Li, H.L., Zhang, Y., Wang, T.T., Feng, S.W., Ren, Q., Cui, Z.B., Cao, C.Y., 2019. Responses of soil denitrifying bacterial communities carrying nirS, nirK, and nosZ genes to revegetation of moving sand dunes. Ecological Indicators107, 105541.

[26] Li, M.N., Li, X.L., Shi, Y.L, Jiang, Y.K., Xue, R.Y., Zhang, Q.W., 2024. Soil enzyme activity mediated organic carbon mineralization due to soil erosion in long gentle sloping farmland in the black soil region. Science of the Total Environment929, 172417.

[27] Liu, B., Mørkved, P.T., Frostegård, Å., Bakken, L.R., 2010. Denitrification gene pools, transcription and kinetics of NO, N₂O and N₂ production as affected by soil pH. FEMS Microbiology Ecology72, 407–417.

[28] Liu, Y., 2009. Influence of Transgenic Populus simoniix Pnigra’s root secretion on soil ecosystem. Northeast Forestry University.

[29] Lu, J.Z., Scheu, S., 2021. Response of soil microbial communities to mixed beech-conifer forests varies with site conditions. Soil Biology and Biochemistry155, 108155.

[30] Miao, X.R., Li, Z.H., Wang, M.Y., Mei, J., Chen, J., 2024. Measurement of cultivated land ecosystem resilience in black soil region of Northeast China under the background of cultivated land protection policy in China: case study of Qiqihar City. Journal of Cleaner Production434, 140141.

[31] Morugán-Coronado, A., Linares, C., Gómez-López, M.D., Faz, Á., Zornoza, R., 2020. The impact of intercropping, tillage and fertilizer type on soil and crop yield in fruit orchards under Mediterranean conditions: a meta-analysis of field studies. Agricultural and Food Sciences, Environmental Science178, 102736.

[32] Ouyang, Y., Evans, S.E., Friesen, M.L., Tiemann, L.K., 2018. Effect of nitrogen fertilization on the abundance of nitrogen cycling genes in agricultural soils: a meta-analysis of field studies. Soil Biology and Biochemistry127, 71–78.

[33] Ramesh, T., Bolan, N.S., Kirkham, M.B., Wijesekara, H., Kanchikerimath, M., Rao, C.S., Sandeep, S., Rinklebe, J., Ok, Y.S., Choudhury, B.U., Wang, H.L., Tan, C.X., Wang, X.J., Song, Z.L., Freeman II, O.W., 2019. Soil organic carbon dynamics: impact of land use changes and management practices: a review. Advances in Agronomy156, 1–107.

[34] Rivest, D., Lorente, M., Olivier, A., Messier, C., 2013. Soil biochemical properties and microbial resilience in agroforestry systems: effects on wheat growth under controlled drought and flooding conditions. Science of the Total Environment 463–464, 463–464.

[35] Schoebitz, M., Castillo, D., Jorquera, M., Roldan, A., 2020. Responses of microbiological soil properties to intercropping at different planting densities in an acidic andisol. Agronomy10, 781.

[36] Shao, M.G., Wang, Y.Q., Xia, Y.Q., Jia, X.X., 2018. Soil drought and water carrying capacity for vegetation in the critical zone of the Loess Plateau: a review. Vadose Zone Journal17, 1539–1566.

[37] Shen, Q., Gao, G.Y., Hu, W., Fu, B.J., 2016. Spatial-temporal variability of soil water content in a cropland-shelterbelt-desert site in an arid inland river basin of Northwest China. Journal of Hydrology540, 873–885.

[38] Shu, X., Daniell, T.J., Hallett, P.D., Baggs, E.M., Griffiths, B.S., 2023. Soil pH moderates the resistance and resilience of C and N cycling to transient and persistent stress. Applied Soil Ecology182, 104690.

[39] Sokol, N.W., Slessarev, E., Marschmann, G.L., Nicolas, A., Blazewicz, S.J., Brodie, E.L., Firestone, M.K., Foley, M.M., Hestrin, R., Hungate, B.A., Koch, B.J., Stone, B.W., Sullivan, M.B., Zablocki, O., Pett-Ridge, J., 2022. Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nature Reviews Microbiology20, 415–430.

[40] Soltangheisi, A., de Moraes, M.T., Cherubin, M.R., Alvarez, D.O., de Souza, L.F., Bieluczyk, W., Navroski, D., Bettoni Teles, A.P., Pavinato, P.S., Martinelli, L.A., Tsai, S.M., de Camargo, P.B., 2019. Forest conversion to pasture affects soil phosphorus dynamics and nutritional status in Brazilian Amazon. Soil and Tillage Research194, 104330.

[41] Spohn, M., Kuzyakov, Y., 2013. Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation-coupling soil zymography with ¹⁴C imaging. Soil Biology and Biochemistry67, 106–113.

[42] Spohn, M., Stendahl, J., 2022. Carbon, nitrogen, and phosphorus stoichiometry of organic matter in Swedish forest soils and its relationship with climate, tree species, and soil texture. Biogeosciences19, 2171–2186.

[43] Tan, H., Barret, M., Mooij, M.J., Rice, O., Morrissey, J.P., Dobson, A., Griffiths, B., O’gara, F., 2013. Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biology and Fertility of Soils49, 661–672.

[44] Wang, B., Zhang, P.J., Zhang, Q.L., 2021. Characteristics of soil aggregates and its influencing factors in Larix gmelinii forest in cold temperate zone. Ecology and Environmental Sciences30, 44–52.

[45] Wang, Q., Zhang, D.Q., F ang W.S., Li, Y., Wang, Q.X., Yan, D.D, Cao, A.C., 2021. Research progress on the effect of soil fumigation on soil nitrogen cycles and functional microorganisms. Chinese Journal of Pesticide Science23, 1063–1072.

[46] Xu, C.H., Xu, X., Ju, C.H., Chen, H.Y.H., Wilsey, B.J., Luo, Y.Q., Fan, W., 2021. Long-term, amplified responses of soil organic carbon to nitrogen addition worldwide. Global Change Biology27, 1170–1180.

[47] Yang, L. P., Chang, H.H., Li, J., Zhang, Z. B., Huang, Y., 2017. Study of the biodiversity in intestinal symbiotic fungi in grasshoppers species by using DNA meta-barcoding. Acta Ecologica Sinica37, 6905–6913.

[48] Ye, L.F., Liu, H.Y., Deng, H.D., Zheng, Y.P., Han, Y.W., Gao, X.T., Abbott, L.K., Zhao, C.M., Li, J.H., 2023. Effects of decadal nitrogen and phosphorus fertilization on microbial taxonomic and functional attributes associated with soil organic carbon decomposition and concentration in an alpine meadow. Ecological Indicators146, 109790.

[49] Yin, L., Dijkstra, F.A., Wang, P., Zhu, B., Cheng, W., 2018. Rhizosphere priming effects on soil carbon and nitrogen dynamics among tree species with and without intraspecific competition. New Phytologist218, 1036–1048.

[50] Yue, K., Fornara, D.A., Li, W., Ni, X.Y., Peng, Y., Liao, S., Tan, S.Y., Wang, D.Y., Wu, F.Z., Yang, Y.S., 2021. Nitrogen addition affects plant biomass allocation but not allometric relationships among different organs across the globe. Journal of Plant Ecology14, 361–371.

[51] Zeng, Z., Hu, Y., Feng, X., Yang, Y., 2019. The diazotrophic community in oat rhizosphere: effects of legume intercropping and crop growth stage. Frontiers of Agricultural Science and Engineering6, 162–171.

[52] Zhang, X., Zhao, Q., Wei, L.M., Sun, Q.Y., Zeng, D.H., 2023. Tree roots exert greater impacts on phosphorus fractions than aboveground litter in mineral soils under a Pinus sylvestris var. mongolica plantation. Forest Ecology and Management545, 121242.

[53] Zou, J., Yao, Q., Liu, J., Li, Y., Song, F., Liu, X., Wang, G., 2020. Changes of diazotrophic communities in response to cropping systems in a mollisol of Northeast China. PeerJ8, e9550.

RIGHTS & PERMISSIONS

Higher Education Press