Elevated CO2 Affects the Soil Organic Carbon Fractions and Their Relation to Soil Microbial Properties in the Rhizosphere of Robinia pseudoacacia L. Seedlings in Cd-Contaminated Soils

Abstract

As the global climates change, elevated CO2 and soil contamination by heavy metal co-occur in natural ecosystems, which are anticipated to affect soil organic carbon fractions (SOC) and their relation to soil microbial activities, but this issue has not been extensively examined. We investigated the response of SOC and their relation with soil microorganisms and enzyme activities in rhizosphere soils of Robinia pseudoacacia L. seedlings to elevated CO2 plus cadmium (Cd) contamination. We found that elevated CO2 significantly (p < 0.05) stimulated total organic carbon (TOC) (8.6%), dissolved organic carbon (DOC) (32.6%), microbial biomass carbon (MBC) (13.5%), bacteria (11.6%), fungi (20.9%), actinomycetes (15.3%), urease (20.1%), dehydrogenase (15.8%), invertase (11.1%), and β-glucosidase (11.9%), and DOC, MBC, bacteria, actinomycetes, urease, and invertase presented smaller growth trend in the range of 500–700 μmol mol−1 CO2 than in the range of 385–500 μmol mol−1 CO2. Cd decreased DOC (30.1%), MBC (24.9%), bacteria (21.5%), actinomycetes (15.9%), and enzyme activities. Elevated CO2 offsets the negative effect of Cd on SOC and microbial activities (except for TOC and L-asparaginase). Procrustes rotation test was used to determine the drivers (elevated CO2, Cd, and CO2 + Cd) of the relation between SOC and microbial activities, revealing the correlations between SOC, soil microorganisms, and enzyme activities were higher under elevated CO2 than under elevated CO2 + Cd. Our results suggest elevated CO2 could stimulate soil fertility and microecological cycle in the rhizosphere microenvironment exposed to heavy metal by affecting the relationship between SOC and soil microbial properties.

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References

  1. A'Bear AD, Jones TH, Kandeler E, Boddy L (2014) Interactive effects of temperature and soil moisture on fungal-mediated wood decomposition and extracellular enzyme activity. Soil Biol Biochem 70:151–158

    CAS  Google Scholar 

  2. Acosta-Martínez V, Cruz L, Sotomayor-Ramírez D, Pérez-Alegría L (2007) Enzyme activities as affected by soil properties and land use in a tropical watershed. Appl Soil Ecol 35:35–45

    Google Scholar 

  3. Ahn MY, Zimmerman AR, Comerford NB, Sickman JO, Grunwald S (2009) Carbon mineralization and labile organic carbon pools in the sandy soils of a North Florida watershed. Ecosystems 12:672–685

    CAS  Google Scholar 

  4. Allard V, Robin C, Newton PCD, Lieffering M, Soussana JF (2006) Short and long-term effects of elevated CO2 on Lolium perenne rhizodeposition and its consequences on soil organic matter turnover and plant N yield. Soil Biol Biochem 36:1178–1187

    Google Scholar 

  5. Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340

    CAS  Google Scholar 

  6. Bhattacharyya P, Roy KS, Neogi S, Manna MC, Adhya TK, Rao KS, Nayak AK (2013) Influence of elevated carbon dioxide and temperature on belowground carbon allocation and enzyme activities in tropical flooded soil planted with rice. Environ Monit Assess 185:8659–8671

    CAS  PubMed  Google Scholar 

  7. Brzezińska M, Włodarczyk T, Stępniewski W, Przywara G (2005) Soil aeration status and catalase activity. Acta Agrophys 5:555–565

    Google Scholar 

  8. Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci 104:4990–4995

    CAS  PubMed  Google Scholar 

  9. Casida LE, Klein D, Santoro T (1964) Soil dehydrogenase activity. Soil Sci 98:371–376

    CAS  Google Scholar 

  10. Chen XM, Liu JX, Deng Q, Yan JH, Zhang DQ (2012) Effects of elevated CO2 and nitrogen addition on soil organic carbon fractions in a subtropical forest. Plant Soil 357:25–34

    CAS  Google Scholar 

  11. Chen P, Liu Q, Liu JY, Jia FA, He XH (2014) Response of soil microbial activity to cadmium pollution and elevated CO2. Sci Rep 4:4287

    PubMed  PubMed Central  Google Scholar 

  12. Cookson WR, Abaye DA, Marschner P, Murphy DV, Stockdale EA, Goulding KW (2005) The contribution of soil organic matter fractions to carbon and nitrogen mineralization and microbial community size and structure. Soil Biol Biochem 37:1726–1737

    CAS  Google Scholar 

  13. D’Aascoli R, Rao MA, Adamo P, Renella G, Landi L, Rutigliano FA et al (2006) Impact of river overflowing on trace element contamination of volcanic soils in South Italy: part II. Soil biological and biochemical properties in relation to trace element speciation. Environ Pollut 144:317–326

    Google Scholar 

  14. De Costa WAJM, Weerakoon WMW, Abeywardena RMI, Herath HMLK (2003a) Response of photosynthesis and water relations of rice (Oryza sativa) to elevated atmospheric carbon dioxide in the subhumid zone of Sri Lanka. J Agron Crop Sci 189:71–82

    Google Scholar 

  15. De Costa WAJM, Weerakoon WMW, Herath HMLK, Abeywardena RMI (2003b) Response of growth and yield of rice (Oryza sativa) to elevated atmospheric elevated atmospheric carbon dioxide in the subhumid zone of Sri Lanka. J Agron Crop Sci 189:83–95

    Google Scholar 

  16. De Costa WAJM, Weerakoon WMW, Herath HMLK, Amaratunga KSP, Abey-wardena RMI (2006) Physiology of yield determination of rice under elevated carbon dioxide at high temperatures in a subhumid tropical climate. Field Crops Res 96:336–347

    Google Scholar 

  17. Deng Q, Cheng XL, Bowatte S, Newton PCD, Zhang QF (2016) Rhizospheric carbon-nitrogen interactions in a mixed-species pasture after 13 years of elevated CO2. Agric Ecosyst Environ 235:134–141

    CAS  Google Scholar 

  18. Ebersberger D, Niklaus PA, Kandeler E (2003) Long term CO2 enrichment stimulates N-mineralisation and enzyme activities in calcareous grassland. Soil Biol Biochem 35:965–972

    CAS  Google Scholar 

  19. Eivazi F, Tabatabai MA (1999) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606

    Google Scholar 

  20. Farrar J, Hawes M, Jones DL, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837

    Google Scholar 

  21. Fliessbach A, Martens R, Reber HH (1994) Soil microbial biomass and microbial activity in soils treated with heavy metal contaminated sewage sludge. Soil Biol Biochem 26:1201–1205

    Google Scholar 

  22. Frankenberger WT, Dick WA (1983) Relationships between enzyme activities and microbial growth and activity indices in soil. Soil Sci Soc Am J 47:945–951

    CAS  Google Scholar 

  23. Frankenberger WT Jr, Tabatabai MA (1991) L-Asparaginase activity of soils. Biol Fertil Soils 11:6–12

    CAS  Google Scholar 

  24. Frostegård Å, Tunlid A, Bååth E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biol Biochem 28:55–63

    Google Scholar 

  25. Gao Y, Zhou P, Mao L, Zhi YE, Zhang CH, Shi WJ (2010) Effects of plant species coexistence on soil enzyme activities and soil microbial community structure under Cd and Pb combined pollution. J Environ Sci 22:1040–1048

    CAS  Google Scholar 

  26. Gianfreda L, Rao MA, Piotrowska A, Palumbo G, Colombo C (2005) Soil enzymes activities as affected by anthropogenic alterations: intensive agricultural practices and organic pollution. Sci Total Environ 341:265–279

    CAS  PubMed  Google Scholar 

  27. Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    CAS  Google Scholar 

  28. Gomes NCM, Landi L, Smalla K, Nannipieri P, Brookes PC, Renella G (2010) Effects of Cd- and Zn-enriched sewage sludge on soil bacterial and fungal communities. Ecotoxicol Environ Saf 73:1255–1263

    CAS  PubMed  Google Scholar 

  29. Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL (2001) Colder soils in a warmer world: a snow manipulation study in northern hardwood forest. Biogeochemistry 56:135–150

    CAS  Google Scholar 

  30. Guo HY, Zhu JG, Zhou H, Sun YY, Ying Y, Pei DP et al (2011) Elevated CO2 levels affects the concentrations of copper and cadmium in crops grown in soil contaminated with heavy metals under fully open-air field conditions. Environ Sci Technol 45:6997–7003

    CAS  PubMed  Google Scholar 

  31. Hassan W, Akmal M, Muhammad I, Younas M, Zahaid KR, Ali F (2013) Response of soil microbial biomass and enzymes activity to cadmium (Cd) toxicity under different soil textures and incubation times. Aust J Crop Sci 7:674–680

    CAS  Google Scholar 

  32. Hofrichter M, Fakoussa R (2001) Microbial degradation and modification of coal. Biopolymers 1:393–429. https://doi.org/10.1007/s42729-020-00205-1

  33. Huang SP, Jia X, Zhao YH, Bai B, Chang YF (2016) Elevated CO2 benefits the soil microenvironment in the rhizosphere of Robinia pseudoacacia L. seedlings in Cd-and Pb-contaminated soils. Chemosphere 168:606–616

    PubMed  Google Scholar 

  34. IPCC (2007) Climate change 2007: the physical science basis, contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  35. Jia X, Wang WK, Chen Z, He YH, Liu JX (2014) Concentrations of secondary metabolites in tissues and root exudates of wheat seedlings changed under elevated atmospheric CO2 and cadmium-contaminated soils. Environ Exp Bot 107:134–143

    CAS  Google Scholar 

  36. Jia X, Liu T, Zhao YH, He YH, Yang MY (2016a) Elevated atmospheric CO2 affected photosynthetic products in wheat seedlings and biological activity in rhizosphere soil under cadmium stress. Environ Sci Pollut Res 23:514–526

    CAS  Google Scholar 

  37. Jia X, Zhao YH, Liu T, Huang SP (2016b) Elevated CO2 affects secondary metabolites in Robinia pseudoacacia L. seedlings in Cd- and Pb-contaminated soil. Chemosphere 160:199–207

    CAS  PubMed  Google Scholar 

  38. Kandeler E, Mosier AR, Morgan JA, Milchunas DG, King JY, Rudolph S, Tscherko D (2006) Response of soil microbial biomass and enzyme activities to the transient elevation of carbon dioxide in a semi-arid grassland. Soil Biol Biochem 38:2448–2460

    CAS  Google Scholar 

  39. Kassem II, Joshi P, Sigler V, Heckathorn S, Wang Q (2008) Effect of elevated CO2 and drought on soil microbial community associated with Andropogon gerardii. J Integr Plant Biol 50:1406–1415

    CAS  PubMed  Google Scholar 

  40. Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595

    CAS  Google Scholar 

  41. Khalid MS, Shaaban M, Hu RG (2019) N2O, CH4, and CO2 emissions from continuous flooded, wet, and flooded converted to wet soils. J Soil Sci Plant Nutr 19:342–351

    CAS  Google Scholar 

  42. Khan MA, Ding X, Khan S, Brusseau ML, Khan A, Nawab J (2018a) The influence of various organic amendments on the bioavailability and plant uptake of cadmium present in mine-degraded soil. Sci Total Environ 636:810–817

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Khan MA, Khan S, Ding X, Khan A, Alam M (2018b) The effects of biochar and rice husk on adsorption and desorption of cadmium on to soils with different water conditions (upland and saturated). Chemosphere 193:1120–1126

    CAS  PubMed  Google Scholar 

  44. Killham K (1985) A physiological determination of the impact of environmental stress on the activity of microbial biomass. Environ Pollut 38:283–294

    CAS  Google Scholar 

  45. Kim S, Kang H (2011) Effects of elevated CO2 and Pb on phytoextraction and enzyme activity. Water Air Soil Pollut 219:365–375

    CAS  Google Scholar 

  46. Klamer M, Roberts MS, Levine LH, Drake BG, Garland JL (2002) Influence of elevated CO2 on the fungal community in a coastal scrub oak forest soil investigated with terminal-restriction fragment length polymorphism analysis. Appl Environ Microbiol 68:4370–4376

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Kools SAE, van Roovert M, van Gestel CAM, van Straalen NM (2005) Glyphosate degradation as a soil health indicator for heavy metal polluted soils. Soil Biol Biochem 37:1303–1307

    CAS  Google Scholar 

  48. Koyama A, Harlow B, Kuske CR, Belnap J, Evans RD (2018) Plant and microbial biomarkers suggest mechanisms of soil organic carbon accumulation in a Mojave Desert ecosystem under elevated CO2. Soil Biol Biochem 120:48–57

    CAS  Google Scholar 

  49. Koyama A, Harlow B, Evans RD (2019) Greater soil carbon and nitrogen in a Mojave Desert ecosystem after 10 years exposure to elevated CO2. Geoderma 355:113915. https://doi.org/10.1016/j.geoderma.2019.113915

    CAS  Article  Google Scholar 

  50. Kuzyakov YV (2001) Tracer studies of carbon translocation by plants from the atmosphere into the soil (a review). Eurasian Soil Sci 34:28–42

    Google Scholar 

  51. Langley JA, McKinley DC, Wolf AA, Hungate BA, Drake BG, Megonigal JP (2009) Priming depletes soil carbon and releases nitrogen in a scrub-oak ecosystem exposed to elevated CO2. Soil Biol Biochem 41:54–60

    CAS  Google Scholar 

  52. Li TQ, Di ZZ, Han X, Yang XE (2012) Elevated CO2 improves root growth and cadmium accumulation in the hyperaccumulator Sedum alfredii. Plant Soil 354:325–334

    CAS  Google Scholar 

  53. Liu XP, Fan YY, Long JX, Wei RF, Kjelgren R, Gong CM et al (2013) Effects of soil water and nitrogen availability on photosynthesis and water use efficiency of Robinia pseudoacacia seedlings. J Environ Sci 25:585–595

    Google Scholar 

  54. Luo Y, Hui DF, Zhang DQ (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63

    PubMed  Google Scholar 

  55. Luo YQ, Zhao XY, Andren O, Zhu YC, Huang WD (2014) Artificial root exudates and soil organic carbon mineralization in a degraded sandy grassland in northern China. J Arid Land 6:423–432

    Google Scholar 

  56. Luo XZ, Hou EQ, Zang XW, Zhang LL, Yi YF, Wen DZ (2019) Effects of elevated atmospheric CO2 and nitrogen deposition on leaf litter and soil carbon degrading enzyme activities in a Cd-contaminated environment: a mesocosm study. Sci Total Environ 671:157–164

    CAS  PubMed  Google Scholar 

  57. Lynch JM, Whipps JM (1991) Substrate flow in the Rhizosphere. Kluwer Academic Publishers, Dordrecht, pp 15–24

    Google Scholar 

  58. Ma SC, Zhang HB, Ma ST, Wang R, Wang GX, Shao Y, Li CX (2015) Effects of mine wastewater irrigation on activities of soil enzymes and physiological properties: heavy metal uptake and grain yield in winter wheat. Ecotoxicol Environ Saf 113:483–490

    CAS  PubMed  Google Scholar 

  59. Ma XY, Liu M, Li ZP (2016) Shifts in microbial biomass and community composition in subtropical paddy soils under a gradient of manure amendment. Biol Fertil Soils 52:775–787

    Google Scholar 

  60. Maenhout P, Van den Bulcke J, Van Hoorebeke L, Cnudde V, De Neve S, Sleutel S (2018) Nitrogen limitations on microbial degradation of plant substrates are controlled by soil structure and moisture content. Front Microbiol 9:1433

    PubMed  PubMed Central  Google Scholar 

  61. Marschner P, Kandeler E, Marschner B (2003) Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461

    CAS  Google Scholar 

  62. Nelson DW, Sommers LE (1982) Total carbon and organic matter (chapter 29). American Society of Agronomy, Inc., Madison, pp 539–577

    Google Scholar 

  63. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, et al (2013) Vegan: community ecology package. R package version 2.0–7

  64. Pan J, Yu L (2011) Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecol Eng 37:1889–1894

    Google Scholar 

  65. Peres-Neto P, Jackson D (2001) How well do multivariate data sets match? The advantages of a procrustean superimposition approach over the Mantel test. Oecologia 129:169–178

    PubMed  Google Scholar 

  66. Renella G, Mench M, Dvander L, Pietramellara G, Ascher J, Ceccherini MT et al (2004) Hydrolase activity, microbial biomass and community structure in long-term Cd-contaminated soils. Soil Biol Biochem 36:44–451

    Google Scholar 

  67. R Core Team (2013) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

  68. Sardar K, Qing C, Hesham AEL, Yue X, Zheng H (2007) Soil enzymatic activities and microbial community structure with different application rates of Cd and Pb. J Environ Sci 19:834–840

    Google Scholar 

  69. Shen GQ, Cao LK, Lu YT, Hong JB (2005) Influence of phenanthrene on cadmium toxicity to soil enzymes and microbial growth. Environ Sci Pollut Res 12:259–263

    CAS  Google Scholar 

  70. Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798

    CAS  PubMed  Google Scholar 

  71. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569

    CAS  Google Scholar 

  72. Sun F, Kuang YW, Wen DZ, Xu DZ, Li JL, Zuo WD, Hou EQ (2010) Long-term tree growth rate, water use efficiency, and tree ring nitrogen isotope composition of Pinus massoniana L. in response to global climate change and local nitrogen deposition in Southern China. J Soil Sediment 10:1453–1465

  73. Tabatabai MA, Bremmer JM (1972) Assay of urease activity in soils. Soil Biol Biochem 4:479–487

    CAS  Google Scholar 

  74. Tripathy S, Bhattacharyya P, Mohapatra R, Som A, Chowdhury D (2014) Influence of different fractions of heavy metals on microbial ecophysiological indicators and enzyme activities in century old municipal solid waste amended soil. Ecol Eng 70:25–34

    Google Scholar 

  75. Uselman SM, Qualls RG, Thomas RB (2000) Effects of increased atmospheric CO2, temperature, and soil N availability on root exudation of dissolved organic carbon by a N-fixing tree (Robinia pseudoacacia L.). Plant Soil 222:191–202

    CAS  Google Scholar 

  76. Ushio M, Kitayama K, Balser TC (2010) Tree species effects on soil enzyme activities through effects on soil physicochemical and microbial properties in a tropical montane forest on Mt. Kinabalu. Borneo Pedobiol 53:227–233

    CAS  Google Scholar 

  77. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    CAS  Google Scholar 

  78. Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135

    CAS  Google Scholar 

  79. Vlachodimos K, Papatheodorou EM, Diamantopouls J, Monokrousos N (2013) Assessment of Robinia pseudoacacia cultivations as a restoration strategy for reclaimed mine spoil heaps. Environ Monit Assess 185:6921–6932

    CAS  PubMed  Google Scholar 

  80. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Wang AS, Angle JS, Chaney RL, Delorme TA, Reeves RD (2006) Soil pH effects on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281:325–337

    CAS  Google Scholar 

  82. Wang D, Heckathorn SA, Barua D, Joshi P, Hamilton EW, LaCroix JJ (2008) Effects of elevated CO2 on the tolerance of photosynthesis to acute heat stress in C3, C4, and CAM species. Am J Bot 95:165–176

    CAS  PubMed  Google Scholar 

  83. Wang YH, Yan DH, Wang JF, Ding Y, Song XS (2017) Effects of elevated CO2 and drought on plant physiology, soil carbon and soil enzyme activities. Pedosphere 27:846–855

    Google Scholar 

  84. Wu HB, Tang SR, Zhang XM, Guo JK, Song ZG, Tian S et al (2009) Using elevated CO2 to increase the biomass of a Sorghum vulgare × Sorghum vulgare var. sudanense hybrid and Trifolium pratense L. and to trigger hyperaccumulation of cesium. J Hazard Mater 170:861–870

    CAS  PubMed  Google Scholar 

  85. Xiao Y, Huang ZG, Lu XG (2015) Changes of soil labile organic carbon fractions and their relation to soil microbial characteristics in four typical wetlands of Sanjiang plain, Northeast China. Ecol Eng 82:381–389

    Google Scholar 

  86. Xu GH, Zheng HY (1986) Handbook of analysis of soil microorganism. Agriculture Press, Beijing, pp 113–116 (249–91)

    Google Scholar 

  87. Xu W, Wang G, Deng F, Zou X, Ruan H, Chen HYH (2018) Responses of soil microbial biomass, diversity and metabolic activity to biochar applications in managed poplar plantations on reclaimed coastal saline soil. Soil Use Manag 34:597–605

    Google Scholar 

  88. Yang QX, Zhang J, Zhu KF, Zhang H (2009) Influence of oxytetracycline on the structure and activity of microbial community in wheat rhizosphere soil. J Environ Sci 7:954–959

    Google Scholar 

  89. Yang YR, Song YY, Scheller HV, Ghosh A, Ban YH, Chen H et al (2015) Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol Biochem 86:146–158

    CAS  Google Scholar 

  90. Yang BS, He F, Zhao XX, Wang H, Xu XH, He XH et al (2019) Composition and function of soil fungal community during the establishment of Quercus acutissima (Carruth.) seedlings in a Cd-contaminated soil. J Environ Manag 246:150–156

    CAS  Google Scholar 

  91. Yuan XX, Lin XG, Chu HY, Yin R, Zhang HY, Hu JL, Zhu JG (2006) Effects of elevated atmospheric CO2 on soil enzyme activities at different nitrogen application treatments. Acta Ecol Sin 26:48–53

    CAS  Google Scholar 

  92. Zaborowska M, Wyszkowska J, Kucharski J (2006) Microbiological activity of zinc-contaminated soils. J Elem 11:543–557

    Google Scholar 

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This study was jointly financed by National Natural Science Foundation of China (grant no. 41807038) and Nanhu Scholars Program for Young Scholars of XYNU.

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Huang, S., Huang, X. & Fang, B. Elevated CO2 Affects the Soil Organic Carbon Fractions and Their Relation to Soil Microbial Properties in the Rhizosphere of Robinia pseudoacacia L. Seedlings in Cd-Contaminated Soils. J Soil Sci Plant Nutr 20, 1203–1214 (2020). https://doi.org/10.1007/s42729-020-00205-1

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Keywords

  • Elevated atmospheric CO2
  • Cd-contaminated soil
  • Soil organic carbon fractions
  • Rhizosphere microbial properties
  • Robinia pseudoacacia L. seedlings