Difference of soil carbon sequestration between rhizosphere and bulk soil in a mountain coniferous forest in southwestern China under nitrogen deposition

doi:10.17521/cjpe.2022.0207

Abstract

Abstract:

Aims Due to complex root-soil interactions, the responses of carbon (C) dynamics in the rhizosphere soil to nitrogen (N) deposition may be different from those in bulk soil. However, the potentially different responses of C dynamics between the rhizosphere and bulk soil and their contributions to soil C sequestration under N deposition are still not elucidated.
Methods In this study, a typical subalpine coniferous plantation (Picea asperata) with chronic N addition treatments in southwestern China was selected as the research object. Based on the experimental plots of simulated N deposition (control: 0 kg·hm^-2·a^-1; N addition: 25 kg·hm^-2·a^-1), we measured the contents of soil organic carbon and its different physical and chemical fractions. Afterwards, by combining the rhizosphere spatial numerical model, we explored the differences in the C pool size of SOC and its fractions and their relative contribution to SOC pools between the rhizosphere and bulk soil, and further quantified the effects of N addition on soil C sequestration in rhizosphere soil.
Important findings The results showed that: 1) Although the addition of N increased the content of SOC and its physical and chemical components in the rhizosphere and non-rhizosphere at the same time, it only reached a significant level in the rhizosphere. Specifically, the rhizosphere SOC content increased by 23.64% under N addition, in which particulate organic carbon (POC), mineral-associated organic carbon (MAOC), labile carbon (LP-C) and recalcitrant carbon (RP-C) content increased by 19.63%, 18.01%, 30.48% and 15.01%, respectively. 2) The total SOC pool increment of spruce forest (0.88 kg·m^-2) was verified with the results of the rhizosphere space numerical model, and the effective rhizosphere extent of the southwest mountain coniferous forest was estimated to be 1.6 mm. Within this extent, N addition increased the SOC stocks of the rhizosphere and bulk soil by 33.37% and 7.38%, contributing to 45.45% and 54.55% of the total SOC pool increment, respectively. Among them, labile C components (POC and LP-C) are the major contributors to rhizosphere SOC accumulation under N addition. These results suggested that the rhizosphere and bulk soil of coniferous forest in southwestern mountainous area had great C sequestration potential under N deposition, and the C sink was more obvious in the rhizosphere soil. Our results highlight the importance of integrating rhizosphere processes into land surface models to accurately predict ecosystem functions in the context of increasing N deposition.

Key words: soil organic carbon, soil carbon fractions, nitrogen deposition, rhizosphere soil, bulk soil, coniferous forest

ZHANG Ying, ZHANG Chang-Hong, WANG Qi-Tong, ZHU Xiao-Min, YIN Hua-Jun. Difference of soil carbon sequestration between rhizosphere and bulk soil in a mountain coniferous forest in southwestern China under nitrogen deposition[J]. Chin J Plant Ecol, 2023, 47(9): 1234-1244.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2022.0207

https://www.plant-ecology.com/EN/Y2023/V47/I9/1234

Figures/Tables 7

Fig. 1 Effects of nitrogen addition on the concentrations of soil organic carbon and its fractions in the rhizosphere and bulk soil in a mountain coniferous forest in southwestern China (mean ± SE). CK, control treatment; N, nitrogen addition treatment. LP-C, labile carbon; MAOC, mineral-associated organic carbon; POC, particulate organic carbon; RP-C, recalcitrant carbon. *, p < 0.05.

Table 1 Extracellular enzyme activities and content of Fe bound in metal-organic complexes in rhizosphere and bulk soil under nitrogen addition and control treatment in a mountain coniferous forest in southwestern China (mean ± SE)

因子 Factor	处理 Treatment	土壤位置 Soil position
因子 Factor	处理 Treatment	根际土壤 Rhizosphere soil	非根际土壤 Bulk soil
β-葡萄糖苷酶活性 BG activity (μmol·h^-1·g^-1 SOC)	CK	1.16 ± 0.14^a	0.54 ± 0.04^a
β-葡萄糖苷酶活性 BG activity (μmol·h^-1·g^-1 SOC)	N	0.81 ± 0.09^b	0.27 ± 0.04^b
多酚氧化酶活性 PPO activity (μmol·h^-1·g^-1 SOC)	CK	35.83 ± 6.97^a	24.84 ± 9.01^a
多酚氧化酶活性 PPO activity (μmol·h^-1·g^-1 SOC)	N	11.58 ± 1.65^b	21.02 ± 4.72^a
金属有机复合体铁离子含量 MOC-Fe content (g·kg^-1)	CK	0.91 ± 0.04^a	0.87 ± 0.02^a
金属有机复合体铁离子含量 MOC-Fe content (g·kg^-1)	N	1.21 ± 0.07^b	0.88 ± 0.04^a

Fig. 2 Results of linear regressions among soil organic carbon (SOC) content and iron ions bound in metal-organic complexes content (A) β-1,4-glucosidase activity (B) and polyphenol oxidase activity (C) in the rhizosphere and bulk soils in a mountain coniferous forest in southwestern China. CKB, bulk soil under control treatment; CKR, rhizosphere under control treatment; NB, bulk soil under nitrogen addition treatment; NR, rhizosphere under nitrogen addition treatment. BG, beta-glucosidase; MOC-Fe, metal-organic complex iron ions; PPO, polyphenol oxidase.

Fig. 3 Total soil organic carbon (SOC) stock (A) and model-simulated SOC stock in rhizosphere and bulk soil (B) under nitrogen addition. 0.5-2.0 mm means root exudates diffusion distance in a mountain coniferous forest in southwestern China (mean ± SE). BS, bulk soil; RS, rhizosphere soil. CK, control treatment; N, nitrogen addition treatment. Different uppercase letters indicate a significant difference of SOC stock in rhizosphere between the control and nitrogen treatments at p < 0.05 level. *, p < 0.05.

Fig. 4 Soil organic carbon (SOC) stock of physical fractions in rhizosphere estimated based on the 1.6 mm rhizosphere extent (A) and its contribution to the increase of total SOC pool (B) in a mountain coniferous forest in southwestern China (mean ± SE). CK, control treatment; N, nitrogen addition treatment. MAOC, mineral-associated organic carbon; POC, particulate organic carbon. *, p < 0.05.

Fig. 5 Soil organic carbon (SOC) stock of chemical fractions in rhizosphere estimated based on the 1.6 mm rhizosphere extent (A) and its contribution to the increase of total SOC pool (B) in a mountain coniferous forest in southwestern China (mean ± SE). CK, control treatment; N, nitrogen addition treatment. LP-C, labile carbon; RP-C, recalcitrant carbon. *, p < 0.05.

Fig. 6 A conceptual framework of how the rhizosphere and bulk soil affect soil carbon sequestration potential in a coniferous forest under nitrogen (N) deposition on the southwest mountain, China. Bsoc, organic carbon stock in bulk soil; LP-C, labile organic carbon pool; MAOC, mineral-associated organic carbon; POC, particulate organic carbon; RP-C, recalcitrant organic carbon pool; Rsoc, organic carbon stock in rhizosphere; SOC, soil organic carbon stock. Solid arrows represent significant responses, and dashed arrows represent non-significant responses.

References 46

[1]	Bonan GB (2008). Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science, 320, 1444-1449.
[2]	Brookes PC, Landman A, Pruden G, Jenkinson DS (1985). Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology & Biochemistry, 17, 837-842. DOI URL
[3]	Brzostek ER, Greco A, Drake JE, Finzi AC (2013). Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry, 115, 65-76. DOI URL
[4]	Carrara JE, Walter CA, Hawkins JS, Peterjohn WT, Averill C, Brzostek ER (2018). Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization. Global Change Biology, 24, 2721-2734. DOI PMID
[5]	Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000). Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology, 81, 2359-2365. DOI URL
[6]	Chen H, Li D, Feng W, Niu S, Plante A, Luo Y, Wang K (2018). Different responses of soil organic carbon fractions additions of nitrogen. European Journal of Soil Science, 69, 1098-1104. DOI URL
[7]	Chen Z, Yin HJ, Wei YY, Liu Q (2010). Short-term effects of night warming and nitrogen addition on soil available nitrogen and microbial properties in subalpine coniferous forest, Western Sichuan, China. Chinese Journal of Plant Ecology, 34, 1254-1264. DOI
	[陈智, 尹华军, 卫云燕, 刘庆 (2010). 夜间增温和施氮对川西亚高山针叶林土壤有效氮和微生物特性的短期影响. 植物生态学报, 34, 1254-1264.] DOI
[8]	Drake JE, Darby BA, Giasson MA, Kramer MA, Phillips RP, Finzi AC (2013). Stoichiometry constrains microbial response to root exudation-insights from a model and a field experiment in a temperate forest. Biogeosciences, 10, 821-838. DOI URL
[9]	Fenn ME, Jovan S, Yuan F, Geiser L, Meixner T, Gimeno BS (2008). Empirical and simulated critical loads for nitrogen deposition in California mixed conifer forests. Environmental Pollution, 155, 492-511. DOI PMID
[10]	Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, Phillips RP (2015). Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Global Change Biology, 21, 2082-2094. DOI PMID
[11]	Gross CD, Harrison RB (2019). The case for digging deeper: soil organic carbon storage, dynamics, and controls in our changing world. Soil Systems, 3, 28. DOI: 10.3390/soilsystems3020028.
[12]	Guenet B, Camino-Serrano M, Ciais P, Tifafi M, Maignan F, Soong JL, Janssens IA (2018). Impact of priming on global soil carbon stocks. Global Change Biology, 24, 1873-1883. DOI PMID
[13]	Guo XM, Wu HH, Luo M, He GP (2007). The morphological change of Fe/Al-oxide minerals in red soils in the process of acidification and its environmental significance. Acta Petrologica et Mineralogica, 26, 515-521.
	[郭杏妹, 吴宏海, 罗媚, 何广平 (2007). 红壤酸化过程中铁铝氧化物矿物形态变化及其环境意义. 岩石矿物学杂志, 26, 515-521.]
[14]	IPCC Intergovernmental Panel on Climate Change (2014). Climate Change 2013—The Physical Science Basis: Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.
[15]	Jian S, Li J, Chen J, Wang G, Mayes MA, Dzantor KE, Hui D, Luo Y (2016). Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: a meta-analysis. Soil Biology & Biochemistry, 101, 32-43. DOI URL
[16]	Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P, Rasche F, Zechmeister-Boltenstern S, Sessitsch A, Richter A (2010). Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytologist, 187, 843-858. DOI PMID
[17]	Keenan RJ, Reams GA, Achard F, de Freitas JV, Grainger A, Lindquist E (2015). Dynamics of global forest area: results from the FAO Global Forest Resources Assessment 2015. Forest Ecology and Management, 352, 9-20. DOI URL
[18]	Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015). Mineral protection of soil carbon counteracted by root exudates. Nature Climate Change, 5, 588-595. DOI
[19]	Kuzyakov Y, Blagodatskaya E (2015). Microbial hotspots and hot moments in soil: concept and review. Soil Biology & Biochemistry, 83, 184-199. DOI URL
[20]	Lehmann J, Kleber M (2015). The contentious nature of soil organic matter. Nature, 528, 60-68. DOI
[21]	Liang C, Schimel JP, Jastrow JD (2017). The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology, 2, 1-6.
[22]	Liu L, Greaver TL (2010). A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecology Letters, 13, 819-828. DOI PMID
[23]	Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013). Enhanced nitrogen deposition over China. Nature, 494, 459-462. DOI
[24]	Lu X, Vitousek PM, Mao Q, Gilliam FS, Luo Y, Turner BL, Zhou G, Mo J (2021). Nitrogen deposition accelerates soil carbon sequestration in tropical forests. Proceedings of the National Academy of Sciences of the United States of America, 118, e2020790118. DOI: 10.1073/pnas.2020790118.
[25]	Lugato E, Lavallee JM, Haddix ML, Panagos P, Cotrufo MF (2021). Different climate sensitivity of particulate and mineral-associated soil organic matter. Nature Geoscience, 14, 295-300. DOI
[26]	Lützow MV, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2006). Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—A review. European Journal of Soil Science, 57, 426-445. DOI URL
[27]	Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P (2004). Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. Forest Ecology & Management, 196, 7-28.
[28]	Meier IC, Pritchard SG, Brzostek ER, McCormack ML, Phillips RP (2015). The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO₂. New Phytologist, 205, 1164-1174. DOI PMID
[29]	Midgley MG, Phillips RP (2016). Resource stoichiometry and the biogeochemical consequences of nitrogen deposition in a mixed deciduous forest. Ecology, 97, 3369-3378. DOI PMID
[30]	Phillips RP, Finzi AC, Bernhardt ES (2011). Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO₂ fumigation. Ecology Letters, 14, 187-194. DOI PMID
[31]	Rovira P, Vallejo VR (2002). Labile and recalcitrant pools of carbon and nitrogen in organic matter decomposing at different depths in soil: an acid hydrolysis approach. Geoderma, 107, 109-141. DOI URL
[32]	Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002). The effects of long-term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry, 34, 1309-1315. DOI URL
[33]	Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011). Persistence of soil organic matter as an ecosystem property. Nature, 478, 49-56. DOI
[34]	Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, et al. (2008). Stoichiometry of soil enzyme activity at global scale. Ecology Letters, 11, 1252-1264. DOI PMID
[35]	Six J, Elliott ET, Paustian K (2000). Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biology & Biochemistry, 32, 2099-2103. DOI URL
[36]	Sokol NW, Bradford MA (2019). Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nature Geoscience, 12, 46-53. DOI
[37]	Sokol NW, Slessarev E, Marschmann GL, Nicolas A, Blazewicz SJ, Brodie EL, Firestone MK, Foley MM, Hestrin R, Hungate BA, Koch BJ, Stone BW, Sullivan MB, Zablocki O, Trubl G, et al. (2022). Life and death in the soil microbiome: How ecological processes influence biogeochemistry. Nature Reviews Microbiology, 20, 415-430. DOI PMID
[38]	Wang J, Liao LR, Wang GL, Liu HF, Wu Y, Liu GB, Zhang C (2022). N-induced root exudates mediate the rhizosphere fungal assembly and affect species coexistence. Science of the Total Environment, 804, 150148.
[39]	Xu ZF, Wan C, Xiong P, Tang Z, Hu R, Cao G, Liu Q (2010). Initial responses of soil CO₂ efflux and C, N pools to experimental warming in two contrasting forest ecosystems, Eastern Tibetan Plateau, China. Plant and Soil, 336, 183-195. DOI URL
[40]	Yan Y, Kuramae EE, de Hollander M, Klinkhamer PGL, van Veen JA (2017). Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere. The ISME Journal, 11, 56-66. DOI
[41]	Yang YH, Shi Y, Sun WJ, Chang JF, Zhu JX, Chen LY, Wang X, Guo YP, Zhang HT, Yu LF, Zhao SQ, Xu K, Zhu JL, Shen HH, Wang YY, et al. (2022). Terrestrial carbon sinks in China and around the world and their contribution to carbon neutrality. Science China: Life Sciences, 65, 861-895. DOI
[42]	Yu G, Jia Y, He N, Zhu J, Chen Z, Wang Q, Piao S, Liu X, He H, Guo X, Wen Z, Li P, Ding G, Goulding K (2019). Stabilization of atmospheric nitrogen deposition in China over the past decade. Nature Geoscience, 12, 424-429. DOI
[43]	Yuan X, Qin WK, Xu H, Zhang ZH, Zhou HK, Zhu B (2020). Sensitivity of soil carbon dynamics to nitrogen and phosphorus enrichment in an alpine meadow. Soil Biology & Biochemistry, 150, 107984. DOI: 10.1016/j.soilbio.2020.107984.
[44]	Zhang ZL, Qiao MF, Li DD, Zhao CZ, Li YJ, Yin HJ, Liu Q (2015). Effects of two root-secreted phenolic compounds from a subalpine coniferous species on soil enzyme activity and microbial biomass. Chemistry and Ecology, 31, 636-649. DOI URL
[45]	Zhu S, Vivanco JM, Manter DK (2016). Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Applied Soil Ecology, 107, 324-333. DOI URL
[46]	Zhu XM, Zhang ZL, Liu DY, Kou YP, Zheng Q, Liu M, Xiao J, Liu Q, Yin HJ (2020). Differential impacts of nitrogen addition on rhizosphere and bulk-soil carbon sequestration in an alpine shrubland. Journal of Ecology, 108, 2309-2320. DOI URL