Journal Home > Volume 9 , Issue 3
Background

Black locust (BL, Robinia pseudoacacia) is considered a promising tree species for reforestation due to its great ability to fix nitrogen. However, after two or three coppice-harvesting rotations, the productivity of BL declines. Whether soil microbial communities are affected and how these groups correlate with the nitrogen mineralization process across multi-generation stands remains unclear.

Methods

We investigated the composition and structure of free-living nitrogen-fixing microorganisms (diazotrophs) by sequencing the marker gene nifH and compared these results to levels of soil nitrogen mineralization in the bulk soil and rhizosphere in black locust plantations on Mount Tai, China.

Results

The results showed multi-generation BL coppice plantations decreased the total soil nitrogen (N), soil phosphorus (P), soil microbial biomass N (MBN), soil microbial biomass C (MBC), soil nitrification rate (Rn), soil ammonification rate (Ra), and net soil N mineralization rate (Rm), but significantly increased the concentration of soil NH4+-N to maintain sufficient NO3-N. The dominant species in bulk soil and rhizosphere changed from Rhodopseudomonas (22.62% and 15.76%), unclassified_c_Alphaproteobacteria (22.37% and 29.28%), unclassified_o_Rhizobiales (15.40% and 13.31%), Bradyrhizobium (12.00% and 11.74%) in seedling plantations to Bradyrhizobium (45.95% and 47.86%) and Rhodopseudomonas (43.56% and 41.84%) in coppice plantations, respectively. Mantel test and Redundancy analysis (RDA) revealed that Rn, Ra, and Rm were the most important factors shaping the diazotrophic communities.

Conclusions

Our results suggest that the multi-generation BL coppice plantation can homogenize soil diazotrophic communities, which is mainly regulated by the available N loss caused by nitrogen mineralization. Strengthening the management technology of coppice plantations will provide more beneficial external consumption.


menu
Abstract
Full text
Outline
About this article

Black locust coppice stands homogenize soil diazotrophic communities by reducing soil net nitrogen mineralization

Show Author's information Kun Lia,1Huimei Tiana,1W. Keith MoserbSteven T. OverbybL. Scott BaggettcRuiqiang Nia( )Chuanrong Lia( )Weixing Shend
Mountain Tai Forest Ecosystem Research Station of State Forestry Administration, Key Laboratory of State Forestry Administration for Silviculture of the Lower Yellow River, Forestry College of Shandong Agricultural University, Tai'an, 271018, Shandong, China
Rocky Mountain Research Station, United States Forest Service, 2500 S. Pine Knoll Dr., Flagstaff, AZ, 86001, USA
Rocky Mountain Research Station, United States Forest Service, 240 West Prospect Fort Collins, CO, 80526, USA
Mount Tai Scenic Spot Management Committee, Tai'an, 271000, Shandong, China

1 Kun Li and Huimei Tian contributed equally to this work.

Abstract

Background

Black locust (BL, Robinia pseudoacacia) is considered a promising tree species for reforestation due to its great ability to fix nitrogen. However, after two or three coppice-harvesting rotations, the productivity of BL declines. Whether soil microbial communities are affected and how these groups correlate with the nitrogen mineralization process across multi-generation stands remains unclear.

Methods

We investigated the composition and structure of free-living nitrogen-fixing microorganisms (diazotrophs) by sequencing the marker gene nifH and compared these results to levels of soil nitrogen mineralization in the bulk soil and rhizosphere in black locust plantations on Mount Tai, China.

Results

The results showed multi-generation BL coppice plantations decreased the total soil nitrogen (N), soil phosphorus (P), soil microbial biomass N (MBN), soil microbial biomass C (MBC), soil nitrification rate (Rn), soil ammonification rate (Ra), and net soil N mineralization rate (Rm), but significantly increased the concentration of soil NH4+-N to maintain sufficient NO3-N. The dominant species in bulk soil and rhizosphere changed from Rhodopseudomonas (22.62% and 15.76%), unclassified_c_Alphaproteobacteria (22.37% and 29.28%), unclassified_o_Rhizobiales (15.40% and 13.31%), Bradyrhizobium (12.00% and 11.74%) in seedling plantations to Bradyrhizobium (45.95% and 47.86%) and Rhodopseudomonas (43.56% and 41.84%) in coppice plantations, respectively. Mantel test and Redundancy analysis (RDA) revealed that Rn, Ra, and Rm were the most important factors shaping the diazotrophic communities.

Conclusions

Our results suggest that the multi-generation BL coppice plantation can homogenize soil diazotrophic communities, which is mainly regulated by the available N loss caused by nitrogen mineralization. Strengthening the management technology of coppice plantations will provide more beneficial external consumption.

Keywords: Soil nutrient, Black locust plantation, nifH gene, Nitrogen mineralization, Coppice

References(88)

Augusto, L., Delerue, F., Gallet-Budynek, A., Achat, D.L., 2013. Global assessment of limitation to symbiotic nitrogen fixation by phosphorus availability in terrestrial ecosystems using a meta-analysis approach. Global Biogeochem. Cycles 27, 804–815. https://doi.org/10.1002/gbc.20069.

Bell, C., Carrillo, Y., Boot, C.M., Rocca, J.D., Pendall, E., Wallenstein, M.D., 2014. Rhizosphere stoichiometry: are C: N: P ratios of plants, soils, and enzymes conserved at the plant species level? New Phytol. 201, 505–517. https://doi.org/10.1111/nph.12531.

Brooks, M.E., Kristensen, K., van Benthem, K.J., Magnusson, A., Berg, C.W., Nielsen, A., Skaug, H.J., Maechler, M., Bolker, B.M., 2017. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. Rev. Javer. 9 (2), 378–400. https://doi.org/10.32614/rj-2017-066.

Booth, M.S., Stark, J.M., Rastetter, E., 2005. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol. Monogr. 75, 139–157. https://doi.org/10.1890/04-0988.

Cai, X., Lin, Z., Penttinen, P., Li, Y., Li, Y., Luo, Y., Yue, T., Jiang, P., Fu, W., 2018. Effects of conversion from a natural evergreen broadleaf forest to a Moso bamboo plantation on the soil nutrient pools, microbial biomass and enzyme activities in a subtropical area. For. Ecol. Manag. 422, 161–171. https://doi.org/10.1016/j.foreco.2018.04.022.

Calderoli, P.A., Collavino, M.M., Behrends Kraemer, F., Morras, H.J.M., Aguilar, O.M., 2017. Analysis of nifH-RNA reveals phylotypes related to Geobacter and Cyanobacteria as important functional components of the N2-fixing community depending on depth and agricultural use of soil. MicrobiologyOpen 6. https://doi.org/10.1002/mbo3.502.

Cao, Y., Zhang, P., Chen, Y., 2017. Soil C: N: P stoichiometry in plantations of N-fixing black locust and indigenous pine, and secondary oak forests in Northwest China. J. Soils Sediments 18, 1478–1489. https://doi.org/10.1007/s11368-017-1884-0.

Carl, C., Biber, P., Veste, M., Landgraf, D., Pretzsch, H., 2018. Key drivers of competition and growth partitioning among Robinia pseudoacacia L. trees. Forest Ecol. Manag. 430, 86–93. https://doi.org/10.1016/j.foreco.2018.08.002.

Carl, C., Lehmann, J., Landgraf, D., Pretzsch, H., 2019. Robinia pseudoacacia L. in short Rotation Coppice: seed and stump shoot reproduction as well as UAS-based spreading analysis. Forests 10 (3), 235. https://doi.org/10.3390/f10030235.

Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, R.K., Ellison, A.M., 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67. https://doi.org/10.1890/13-0133.1.

Chapin III, F.S., Matson, P.A., Vitousek, P., 2011. Principles of Terrestrial Ecosystem Ecology. Springer Science & Business Media, New York.
DOI

Che, R.X., Deng, Y.C., Wang, F., Wang, W.J., Xu, Z.H., Hao, Y.B., Xue, K., Zhang, B., Tang, L., Zhou, H.K., Cui, X.Y., 2018. Autotrophic and symbiotic diazotrophs dominate nitrogen-fixing communities in Tibetan grassland soils. Sci. Total Environ. 639, 997–1006. https://doi.org/10.1016/j.scitotenv.2018.05.238.

Chen, J., Shen, W.J., Xu, H., Li, Y.D., Luo, T.S., 2019a. The composition of nitrogen-fixing microorganisms correlates with soil nitrogen content during reforestation: a comparison between legume and non-legume plantations. Front. Microbiol. 10, 508. https://doi.org/10.3389/fmicb.2019.00508.

Chen, J., Wang, P., Wang, C., Wang, X., Miao, L., Liu, S., Yuan, Q., 2019b. Dam construction alters function and community composition of diazotrophs in riparian soils across an environmental gradient. Soil Biol. Biochem. 132, 14–23. https://doi.org/10.1016/j.soilbio.2019.01.020.

Cierjacks, A., Kowarik, I., Joshi, J., Hempel, S., Ristow, M., von der Lippe, M., Weber, E., 2013. Biological flora of the British isles: Robinia pseudoacacia. J. Ecol. 101, 1623–1640. https://doi.org/10.1111/1365-2745.12162.

DeLuca, T.H., Drinkwater, L.E., Wiefling, B.A., DeNicola, D.M., 1996. Free-living nitrogen-fixing bacteria in temperate cropping systems: influence of nitrogen source. Biol. Fertil. Soils 23, 140–144. https://doi.org/10.1007/BF00336054.

Fan, K.K., Weisenhorn, P., Gilbert, J.A., Shi, Y., Bai, Y., Chu, H.Y., 2018. Soil pH correlates with the co-occurrence and assemblage process of diazotrophic communities in rhizosphere and bulk soils of wheat fields. Soil Biol. Biochem. 121, 185–192. https://doi.org/10.1016/j.soilbio.2018.03.017.

Fu, W., Wang, X., Wei, X.R., 2019. No response of soil N mineralization to experimental warming in a northern middle-high latitude agro-ecosystem. Sci. Total Environ. 659, 240–248. https://doi.org/10.1016/j.scitotenv.2018.12.315.

Gaby, J.C., Buckley, D.H., 2011. A global census of nitrogenase diversity. Environ. Microbiol. 13 (7), 1790–1799. https://doi.org/10.1111/j.1462-2920.2011.02488.x.

Gaby, J.C., Buckley, D.H., 2014. A Comprehensive Aligned nifH Gene Database: a Multipurpose Tool for Studies of Nitrogen-Fixing Bacteria. Database. https://doi.org/10.1093/database/bau001,2014.
DOI

Geisseler, D., Horwath, W.R., Joergensen, R.G., Ludwig, B., 2010. Pathways of nitrogen utilization by soil microorganisms – a review. Soil Biol. Biochem. 42, 2058–2067. https://doi.org/10.1016/j.soilbio.2010.08.021.

Guillaume, T., Kotowska, M.M., Hertel, D., Knohl, A., Krashevska, V., Murtilaksono, K., Scheu, S., Kuzyakov, Y., 2018. Carbon costs and benefits of Indonesian rainforest conversion to plantations. Nat. Commun. 9, 2388. https://doi.org/10.1038/s41467-018-04755-y.

Hart, S.C., Stark, J.M., Davidson, E.A., Firestone, M.K., 1994. Nitrogen mineralization, immobilization, and nitrification. Methods of Soil Analysis: Part 2 Microbiological and Biochemical Properties 5, 985–1018. https://doi.org/10.2136/sssabookser5.2.c42.

Hill, M., 1973. Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432. https://doi.org/10.2307/1934352.

Hoogmoed, M., Cunningham, S.C., Baker, P.J., Beringer, J., Cavagnaro, T.R., 2014. Is there more soil carbon under nitrogen-fixing trees than under non-nitrogen-fixing trees in mixed-species restoration plantings? Agric. Ecosyst. Environ. 188, 80–84. https://doi.org/10.1016/j.agee.2014.02.013.

Hsu, S.F., Buckley, D.H., 2009. Evidence for the functional significance of diazotroph community structure in soil. ISME J. 3, 124–136. https://doi.org/10.1038/ismej.2008.82.

Hu, X.J., Liu, J.J., Zhu, P., Wei, D., Jin, J., Liu, X.B., Wang, G.H., 2018. Long-term manure addition reduces diversity and changes the community structure of diazotrophs in a neutral black soil of northeast China. J. Soils Sediments 18, 2053–2062. https://doi.org/10.1007/s11368-018-1975-6.

Kerfahi, D., Tripathi, B.M., Dong, K., Go, R., Adams, J.M., 2016. Rainforest conversion to rubber plantation may not result in lower soil diversity of bacteria, fungi, and nematodes. Microb. Ecol. 72, 359–371. https://doi.org/10.1007/s00248-016-0790-0.

Kong, W.B., Yao, Y.F., Zhao, Z.N., Qin, X., Zhu, H.S., Wei, X.R., Shao, M.A., Wang, Z., Bao, K.Q., Su, M., 2019. Effects of vegetation and slope aspect on soil nitrogen mineralization during the growing season in sloping lands of the Loess Plateau. Catena 172, 753–763. https://doi.org/10.1016/j.catena.2018.09.037.

Koponen, P., Nygren, P., Domenach, A.M., Le Roux, C., Saur, E., Roggy, J.C., 2003. Nodulation and dinitrogen fixation of legume trees in a tropical freshwater swamp forest in French Guiana. J. Trop. Ecol. 19, 655–666. https://doi.org/10.1017/S0266467403006059.

Kramer, C.Y., 1956. Extension of multiple range tests to group means with unequal numbers of replications. Int. Biomet. Soc. 12, 307–310. https://doi.org/10.2307/3001469.

LeBauer, D.S., Treseder, K.K., 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379. https://doi.org/10.1890/06-2057.1.

Lenth, R.V., 2021. Emmeans: Estimated Marginal Means, Aka Least-Squares Means. R Package Version 1.6.0. https://CRAN.R-project.org/package=emmeans.

Li, D.J., Niu, S.L., Luo, Y.Q., 2012. Global patterns of the dynamics of soil carbon and nitrogen stocks following afforestation: a meta-analysis. New Phytol. 195, 172–181. https://doi.org/10.1111/j.1469-8137.2012.04150.x.

Li, K., Han, X., Ni, R.Q., Shi, G., de-Miguel, S., Li, C.R., Shen, W.X., Zhang, Y.K., Zhang, X.Z., 2021. Impact of Robinia pseudoacacia stand conversion on soil properties and bacterial community composition in Mount Tai, China. Forest Ecosyst. 8, 19. https://doi.org/10.1186/s40663-021-00296-x.

Li, Z.L., Tian, D.S., Wang, B.X., Wang, J.S., Wang, S., Chen, H.Y.H., Xu, X.F., Wang, C.H., He, N.P., Niu, S.L., 2019. Microbes drive global soil nitrogen mineralization and availability. Global Change Biol. 25, 1078–1088. https://doi.org/10.1111/gcb.14557.

Li, Z.L., Zeng, Z.Q., Tian, D.S., Wang, J.S., Fu, Z., Wang, B.X., Tang, Z., Chen, W.N., Chen, H.Y.H., Wang, C.H., Yi, C.X., Niu, S.L., 2020. The stoichiometry of soil microbial biomass determines metabolic quotient of nitrogen mineralization. Environ. Res. Lett. 15 (3), 034005. https://doi.org/10.1088/1748-9326/ab6a26.

Liu, X.Y., Liu, C., Gao, W.H., Xue, C., Guo, Z.H., Jiang, L., Li, F., Liu, Y., 2019. Impact of biochar amendment on the abundance and structure of diazotrophic community in an alkaline soil. Sci. Total Environ. 688, 944–951. https://doi.org/10.1016/j.scitotenv.2019.06.293.

Margesin, R., Schinner, F., 2005. Manual for Soil Analysis-Monitoring and Assessing Soil Bioremediation. Springer Science & Business Media, New York.
DOI

Medina-Villar, S., Rodríguez-Echeverría, S., Lorenzo, P., Alonso, A., Pérez-Corona, E., Castro-Díez, P., 2016. Impacts of the alien trees Ailanthus altissima (Mill.) Swingle and Robinia pseudoacacia L. on soil nutrients and microbial communities. Soil Biol. Biochem. 96, 65–73. https://doi.org/10.1016/j.soilbio.2016.01.015.

Meng, H., Wu, R.N., Wang, Y.F., Gu, J.D., 2017. A comparison of denitrifying bacterial community structures and abundance in acidic soils between natural forest and revegetated forest of Nanling Nature Reserve in southern China. J. Environ. Manag. 198, 41–49. https://doi.org/10.1016/j.jenvman.2017.04.066.

Meng, H., Zhou, Z.C., Wu, R.N., Wang, Y.F., Gu, J.D., 2019. Diazotrophic microbial community and abundance in acidic subtropical natural and re-vegetated forest soils revealed by high-throughput sequencing of nifH gene. Appl. Microbiol. Biotechnol. 103, 995–1005. https://doi.org/10.1007/s00253-018-9466-7.

Meng, Y., Cao, B.H., Mao, P.L., Dong, C., Cao, X.D., Qi, L., Wang, M.X., Wu, Y., 2020. Tree species distribution change study in Mount Tai based on Landsat remote sensing image data. Forests 11 (2), 130. https://doi.org/10.3390/f11020130.

Mirza, B.S., Potisap, C., Nusslein, K., Bohannan, B.J., Rodrigues, J.L., 2014. Response of free-living nitrogen-fixing microorganisms to land-use change in the Amazon rainforest. Appl. Environ. Microbiol. 80, 281–288. https://doi.org/10.1128/AEM.02362-13.

Moghimian, N., Hosseini, S.M., Kooch, Y., Darki, B.Z., 2017. Impacts of changes in land use/cover on soil microbial and enzyme activities. Catena 157, 407–414. https://doi.org/10.1016/j.catena.2017.06.003.

Murphy, C.J., Baggs, E.M., Morley, N., Wall, D.P., Paterson, E., 2017. Nitrogen availability alters rhizosphere processes mediating soil organic matter mineralisation. Plant Soil 417, 499–510. https://doi.org/10.1007/s11104-017-3275-0.

Ng, E.L., Patti, A.F., Rose, M.T., Schefe, C.R., Wilkinson, K., Cavagnaro, T.R., 2014. Functional stoichiometry of soil microbial communities after amendment with stabilised organic matter. Soil Biol. Biochem. 76, 170–178. https://doi.org/10.1016/j.soilbio.2014.05.016.

Nie, H.J., Qin, T.L., Yan, D.H., Lv, X.Z., Wang, J.W., Huang, Y.H., Lv, Z.Y., Liu, S.S., Liu, F., 2021. How do tree species characteristics affect the bacterial community structure of subtropical natural mixed forests? Sci. Total Environ. 764, 144633. https://doi.org/10.1016/j.scitotenv.2020.144633.

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 Biol. Biochem. 127, 71–78. https://doi.org/10.1016/j.soilbio.2018.08.024.

Peerawat, M., Blaud, A., Trap, J., Chevallier, T., Alonso, P., Gay, F., Thaler, P., Spor, A., Sebag, D., Choosai, C., Suvannang, N., Sajjaphan, K., Brauman, A., 2018. Rubber plantation ageing controls soil biodiversity after land conversion from cassava. Agric. Ecosyst. Environ. 257, 92–102. https://doi.org/10.1016/j.agee.2018.01.034.

Petersen, D.G., Blazewicz, S.J., Firestone, M., Herman, D.J., Turetsky, M., Waldrop, M., 2012. Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ. Microbiol. 14, 993–1008. https://doi.org/10.1111/j.1462-2920.2011.02679.x.

Pogoreutz, C., Radecker, N., Cardenas, A., Gardes, A., Wild, C., Voolstra, C.R., 2017. Nitrogen Fixation Aligns with nifH abundance and expression in two coral trophic functional groups. Front. Microbiol. 8, 1187. https://doi.org/10.3389/fmicb.2017.01187.

R Core Team, 2021. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. (Accessed 10 April 2021).

Rachid, C.T.C.C., Balieiro, F.C., Peixoto, R.S., Pinheiro, Y.A.S., Piccolo, M.C., Chaer, G.M., Rosado, A.S., 2013. 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.

Rahman, M.M., Bárcena, T.G., Vesterdal, L., 2017. Tree species and time since afforestation drive soil C and N mineralization on former cropland. Geoderma 305, 153–161. https://doi.org/10.1016/j.geoderma.2017.06.002.

Reed, S.C., Cleveland, C.C., Townsend, A.R., 2011. Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu. Rev. Ecol. Evol. Syst. 42, 489–512. https://doi.org/10.1146/annurev-ecolsys-102710-145034.

Rigby, H., Clarke, B.O., Pritchard, D.L., Meehan, B., Beshah, F., Smith, S.R., Porter, N.A., 2016. A critical review of nitrogen mineralization in biosolids-amended soil, the associated fertilizer value for crop production and potential for emissions to the environment. Sci. Total Environ. 541, 1310–1338. https://doi.org/10.1016/j.scitotenv.2015.08.089.

Rodrigues, J.L.M., Pellizari, V.H., Mueller, R., Baek, K., Jesus, E. d. C., Paula, F.S., Mirza, B., Hamaoui, G.S., Tsai, S.M., Feigl, B., Tiedje, J.M., Bohannan, B.J.M., Nüsslein, Klaus, 2013. Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc. Natl. Acad. Sci. U. S. A 110 (3), 988–993. https://doi.org/10.1073/pnas.1220608110.

Rodríguez-Blanco, A., Sicardi, M., Frioni, L., 2015. Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biol. Fertil. Soils 51, 391–402. https://doi.org/10.1007/s00374-014-0986-8.

Saleem, M., Law, A.D., Sahib, M.R., Pervaiz, Z.H., Zhang, Q.M., 2018. Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere 6, 47–51. https://doi.org/10.1016/j.rhisph.2018.02.003.

Sánchez, C., Tortosa, G., Granados, A., Delgado, A., Bedmar, E.J., Delgado, M.J., 2011. Involvement of Bradyrhizobium japonicum denitrification in symbiotic nitrogen fixation by soybean plants subjected to flooding. Soil Biol. Biochem. 43, 212–217. https://doi.org/10.1016/j.soilbio.2010.09.020.

Schmidt, J., Fester, T., Schulz, E., Michalzik, B., Buscot, F., Gutknecht, J., 2017. Effects of plant-symbiotic relationships on the living soil microbial community and microbial necromass in a long-term agro-ecosystem. Sci. Total Environ. 581–582, 756–765. https://doi.org/10.1016/j.scitotenv.2017.01.005.

Stewart, K.J., Coxson, D., Siciliano, S.D., 2011. Small-scale spatial patterns in N2-fixation and nutrient availability in an arctic hummock–hollow ecosystem. Soil Biol. Biochem. 43, 133–140. https://doi.org/10.1016/j.soilbio.2010.09.023.

Straub, K.L., Schönhuber, W.A., Buchholz-Cleven, B.E.E., Schink, B., 2004. Diversity of ferrous iron-oxidizing, nitrate-reducing bacteria and their involvement in oxygenindependent iron cycling. Geomicrobiol. J. 21, 371–378. https://doi.org/10.1080/01490450490485854.

Tang, Y.F., Zhang, M.M., Chen, A.L., Zhang, W.Z., Wei, W.X., Sheng, R., 2017. Impact of fertilization regimes on diazotroph community compositions and N2-fixation activity in paddy soil. Agric. Ecosyst. Environ. 247, 1–8. https://doi.org/10.1016/j.agee.2017.06.009.

Thapa, R., Tully, K.L., Cabrera, M.L., Dann, C., Schomberg, H.H., Timlin, D., RebergHorton, C., Gaskin, J., Davis, B.W., Mirsky, S.B., 2021. Effects of moisture and temperature on C and N mineralization from surface-applied cover crop residues. Biol. Fertil. Soils 57, 485–498. https://doi.org/10.1007/s00374-021-01543-7.

Tian, D., Jiang, L., Ma, S.H., Fang, W.J., Schmid, B., Xu, L.C., Zhu, J.X., Li, P., Losapio, G., Jing, X., Zheng, C.Y., Shen, H.H., Xu, X.N., Zhu, B., Fang, J.Y., 2017. Effects of nitrogen deposition on soil microbial communities in temperate and subtropical forests in China. Sci. Total Environ. 607–608, 1367–1375. https://doi.org/10.1016/j.scitotenv.2017.06.057.

Urakawa, R., Ohte, N., Shibata, H., Isobe, K., Tateno, R., Oda, T., Hishi, T., Fukushima, K., Inagaki, Y., Hirai, K., Oyanagi, N., Nakata, M., Toda, H., Kenta, T., Kuroiwa, M., Watanabe, T., Fukuzawa, K., Tokuchi, N., Ugawa, S., Enoki, T., Nakanishi, A., Saigusa, N., Yamao, Y., Kotani, A., 2016. Factors contributing to soil nitrogen mineralization and nitrification rates of forest soils in the Japanese archipelago. For. Ecol. Manag. 361, 382–396. https://doi.org/10.1016/j.foreco.2015.11.033.

Usman, S., Singh, S.P., Rawat, Y.S., 2000. Nitrification mineralisation and inorganic-N uptake in evergreen forests of the central Himalayas. Eur. J. Soil Biol. 36 (2), 65–71. https://doi.org/10.1016/S1164-5563(00)01053-0.

Vitali, F., Mastromei, G., Senatore, G., Caroppo, C., Casalone, E., 2016. Long-lasting effects of the conversion from natural forest to poplar plantation on soil microbial communities. Microbiol. Res. 182, 89–98. https://doi.org/10.1016/j.micres.2015.10.002.

Wang, C., Liu, D.W., Bai, E., 2018a. Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biol. Biochem. 120, 126–133. https://doi.org/10.1016/j.soilbio.2018.02.003.

Wang, C., Zheng, M.M., Song, W.F., Wen, S.L., Wang, B.R., Zhu, C.Q., Shen, R.F., 2017. Impact of 25 years of inorganic fertilization on diazotrophic abundance and community structure in an acidic soil in southern China. Soil Biol. Biochem. 113, 240–249. https://doi.org/10.1016/j.soilbio.2017.06.019.

Wang, C., Zheng, M.M., Chen, J., Shen, R.F., 2021. Land-use change has a greater effect on soil diazotrophic community structure than the plant rhizosphere in acidic ferralsols in southern China. Plant Soil 462, 445–458. https://doi.org/10.1007/s11104-021-04883-3.

Wang, Q., Wang, J.L., Li, Y.Z., Chen, D.W., Ao, J.H., Zhou, W.L., Shen, D.C., Li, Q.W., Huang, Z.R., Jiang, Y., 2018b. Influence of nitrogen and phosphorus additions on N2-fixation activity, abundance, and composition of diazotrophic communities in a Chinese fir plantation. Sci. Total Environ. 619–620, 1530–1537. https://doi.org/10.1016/j.scitotenv.2017.10.064.

Wei, X.R., Shao, M.A., Fu, X.L., Ågren, G.I., Yin, X.Q., 2011. The effects of land use on soil N mineralization during the growing season on the northern Loess Plateau of China. Geoderma 160, 590–598. https://doi.org/10.1016/j.geoderma.2010.11.007.

Westfall, P.H., Young, S.S., 1993. Resampling-based Multiple Testing: Examples and Methods for P-Value Adjustment. John Wiley & Sons, New York.

Wood, S.A., Gilbert, J.A., Leff, J.W., Fierer, N., D'Angelo, H., Bateman, C., Gedallovich, S.M., Gillikin, C.M., Gradoville, M.R., Mansor, P., Massmann, A., Yang, N., Turner, B.L., Brearley, F.Q., McGuire, K.L., 2017. Consequences of tropical forest conversion to oil palm on soil bacterial community and network structure. Soil Biol. Biochem. 112, 258–268. https://doi.org/10.1016/j.soilbio.2017.05.019.

Wu, H., Cai, A., Xing, T., Huai, S., Zhu, P., Xu, M., Lu, C., 2021. Fertilization enhances mineralization of soil carbon and nitrogen pools by regulating the bacterial community and biomass. J. Soils Sediments 21, 1633–1643. https://doi.org/10.1007/s11368-020-02865-z.

Xu, Y.D., Wang, T., Li, H., Ren, C.J., Chen, J.W., Yang, G.H., Han, X.H., Feng, Y.Z., Ren, G.X., Wang, X.J., 2019. Variations of soil nitrogen-fixing microorganism communities and nitrogen fractions in a Robinia pseudoacacia chronosequence on the Loess Plateau of China. Catena 174, 316–323. https://doi.org/10.1016/j.catena.2018.11.009.

Xu, Z.F., Hu, R., Xiong, P., Wan, C., Cao, G., Liu, Q., 2010. Initial soil responses to experimental warming in two contrasting forest ecosystems, Eastern Tibetan Plateau, China: nutrient availabilities, microbial properties and enzyme activities. Appl. Soil Ecol. 46, 291–299. https://doi.org/10.1016/j.apsoil.2010.07.005.

Yang, K., Zhu, J.J., Xu, S., Zheng, X., 2018. Conversion from temperate secondary forests into plantations (Larix spp.): impact on belowground carbon and nutrient pools in northeastern China. Land Degrad. Dev. 29, 4129–4139. https://doi.org/10.1002/ldr.3169.

Yang, K., Zhu, J.J., Zhang, M., Yan, Q., Sun, O.J., 2010. Soil microbial biomass carbon and nitrogen in forest ecosystems of Northeast China: a comparison between natural secondary forest and larch plantation. J. Plant Ecol. 3, 175–182. https://doi.org/10.1093/jpe/rtq022.

Yang, Y.H., Luo, Y.Q., Finzi, A.C., 2011. Carbon and nitrogen dynamics during forest stand development: a global synthesis. New Phytol. 190, 977–989. https://doi.org/10.1111/j.1469-8137.2011.03645.x.

Yao, Y.F., Zhao, Z.N., Wei, X.R., Shao, M.A., 2019. Effects of shrub species on soil nitrogen mineralization in the desert-loess transition zone. Catena 173, 330–338. https://doi.org/10.1016/j.catena.2018.10.016.

Zhang, M.Y., Wang, W.J., Wang, D.J., Heenan, M., Xu, Z.H., 2018. Short-term responses of soil nitrogen mineralization, nitrification, and denitrification to prescribed burning in a suburban forest ecosystem of subtropical Australia. Sci. Total Environ. 642, 879–886. https://doi.org/10.1016/j.scitotenv.2018.06.144.

Zhang, Y.H., Xu, X.J., Li, Y., Huang, L.D., Xie, X.J., Dong, J.M., Yang, S.Q., 2016. Effects of Spartina alterniflora invasion and exogenous nitrogen on soil nitrogen mineralization in the coastal salt marshes. Ecol. Eng. 87, 281–287. https://doi.org/10.1016/j.ecoleng.2015.12.003.

Zhao, J.W., Tao, Q., Li, B., Luo, J.P., Zhang, H.Y., Lu, C.L., Li, Q.Q., Xu, Q., Huang, R., Li, H.X., Li, B., Chen, Y.L., Wang, C.Q., 2021. Low-pyrolysis-temperature biochar promoted free-living N2-fixation in calcareous purple soil by affecting diazotrophic composition. Geoderma 388, 114969. https://doi.org/10.1016/j.geoderma.2021.114969.

Zhou, L.T., Li, J.J., Pokhrel, G.R., Chen, J., Zhao, Y.L., Bai, Y., Zhang, C., Lin, W.X., Wu, Z.Y., Wu, C.Z., 2021. nifH Gene sequencing reveals the effects of successive monoculture on the soil diazotrophic microbial community in Casuarina equisetifolia plantations. Front. Plant Sci. 11, 578812. https://doi.org/10.3389/fpls.2020.578812.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 22 January 2022
Revised: 02 March 2022
Accepted: 10 March 2022
Published: 06 April 2022
Issue date: June 2022

Copyright

© 2022 The Authors.

Acknowledgements

We are very grateful to all the students who assisted with data collection and the experiments. We also thank three anonymous reviewers for their helpful comments and suggestions on this paper.

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return