Abstract
An experiment was conducted with tobacco (Nicotiana tabacum L.) grown in a Cd- and Pb-contaminated calcareous soil amended with 0.0, 1.0, 2.5, and 5.0% (w/w) tobacco stalk biochar (BC). The BC amendment significantly increased organic matter, total C, N, P, and K contents of soil, and the C/N ratio. Bioavailable metal concentrations (DTPA extraction) decreased by increasing BC application rate. The 5.0% BC amendment significantly decreased the DTPA-extractable Cd and Pb by 10.4 and 13.6%, respectively. Correspondingly, the bioaccumulation and translocation factors of Cd and Pb also decreased by increasing the BC addition rates and this indicated that BC inhibited the uptake and transfer of both Cd and Pb by tobacco plants. Moreover, high-throughput sequencing revealed that BC increased Chao1 richness, Shannon’s diversity and Simpson’s diversity of bacterial communities of soil. The relative abundance and genera composition of Adhaeribacter, Rhodoplanes, Pseudoxanthomonas, and Candidatus Xiphinematobacter increased under BC treatments, while those of Kaistobacter, Lacibacter, and Pirellula decreased. Overall, BC increased soil nutrients (C, N, P, and K contents), enhanced bacterial diversity indexes and richness, and changed the bacterial community composition, which may all have contributed to reduce the mobility and bioavailability of both Cd and Pb in a calcareous soil.
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References
Acosta-Martinez V, Dowd SE, Sun Y, Wester D, Allen V (2010) Pyrosequencing analysis for characterization of soil bacterial populations as affected by an integrated livestock-cotton production system. Appl Soil Ecol 45(1):13–25. https://doi.org/10.1016/j.apsoil.2010.01.005
Ahmad M, Ok YS, Kim BY, Ahn JH, Lee YH, Zhang M, Moon DH, Al-Wabel MI, Lee SS (2016) Impact of soybean stover- and pine needle-derived biochars on Pb and As mobility, microbial community, and carbon stability in a contaminated agricultural soil. J Environ Manag 166:131–139. https://doi.org/10.1016/j.jenvman.2015.10.006
Ai BL, Sheng ZW, Zheng LL, Shang WT (2015) Collectable amounts of straw resources and their distribution in China. In: Proceedings of the International Conference on Advances in Energy, Environ Chem Eng volume:441–444
Akesson A, Bjellerup P, Lundh T, Lidfeldt J, Nerbrand C, Samsioe G, Skerfving S, Vahter M (2006) Cadmium-induced effects on bone in a population-based study of women. Environ Health Perspect 114(6):830–834. https://doi.org/10.1289/ehp.8763
Al-Farraj AS, Al-Wabel MI, Al-Shahrani TS, El-Maghraby SE, Al-Sewailem MAS (2010) Accumulation coefficient and translocation factor of heavy metals through Rhazya stricta grown in the mining area of Mahad AD'Dahab, Saudi Arabia. WIT Trans Ecol Environ 140:325–336
Allen SE, Grimshaw HM, Rowland AP (1986) Chemical analysis. In: Moore PD, Chapman SB (eds) Methods in plant ecology. Blackwell Scientific Publication, Oxford, London, pp 285–344
Allison LE (1965) Organic carbon. In: Black CA, Evans DD, White JL, Ensminger LE, Clark FE (Eds) Methods of Soil Analysis. Am Soc Agron, Madison, WI, pp 1367–1389
Angelova V, Ivanov K, Ivanova R (2004) Effect of chemical forms of lead, cadmium, and zinc in polluted soils on their uptake by tobacco. J Plant Nutr 27:757–773. https://doi.org/10.1081/PLN-120030609
Beesley L, Marmiroli M (2011) The immobilisation and retention of soluble arsenic, cadmium and zinc by biochar. Environ Pollut 159(2):474–480. https://doi.org/10.1016/j.envpol.2010.10.016
Bellinger DC (2008) Very low lead exposures and children's neurodevelopment. Curr Opin Pediatr 20(2):172–177. https://doi.org/10.1097/MOP.0b013e3282f4f97b
Bian RJ, Joseph S, Cui LQ, Pan GX, Li LQ, Liu XY, Zhang A, Rutlidge H, Wong SW, Chia C, Marjo C, Gong B, Munroe P, Donne S (2014) A three-year experiment confirms continuous immobilization of cadmium and lead in contaminated paddy field with biochar amendment. J Hazard Mater 272:121–128. https://doi.org/10.1016/j.jhazmat.2014.03.017
Bird MI, Wurster CM, Silva PHD, Paul NA, de Nys R (2012) Algal biochar: effects and applications. Glob Change Biol Bioenergy 4(1):61–69. https://doi.org/10.1111/j.1757-1707.2011.01109.x
Budai A, Rasse DP, Lagomarsino A, Lerch TZ, Paruch L (2016) Biochar persistence, priming and microbial responses to pyrolysis temperature series. Biol Fertil Soils 52(6):749–761. https://doi.org/10.1007/s00374-016-1116-6
Burzynski M, Klobus G (2004) Changes of photosynthetic parameters in cucumber leaves under cu, cd, and Pb stress. Photosynthetica 42(4):505–510. https://doi.org/10.1007/S11099-005-0005-2
Cao XD, Ma LQ (2004) Effects of compost and phosphate on plant arsenic accumulation from soils near pressure-treated wood. Environ Pollut 132(3):435–442. https://doi.org/10.1016/j.envpol.2004.05.019
Chaney RL, Reeves PG, Ryan JA, Simmons RW, Welch RM, Angle JS (2004) An improved understanding of soil cd risk to humans and low cost methods to phytoextract Cd from contaminated soils to prevent soil cd risks. Biometals 17(5):549–553. https://doi.org/10.1023/B:BIOM.0000045737.85738.cf
Chintala R, Schumacher TE, McDonald LM, Clay DE, Malo DD, Papiernik SK, Clay SA, Julson J (2014) Phosphorus sorption and availability from biochars and soil/biochar mixtures. Clean-Soil Air Water 42(5):626–634. https://doi.org/10.1002/clen.201300089
del Piano L, Abet M, Sorrentino C, Barbato L, Sicignano M, Cozzolino E, Cuciniello A (2008) Uptake and distribution of lead in tobacco (Nicotiana tabacum L.) J Appl Bot Food Qual 82(1):21–25
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Gregory SJ, Anderson CWN, Camps-Arbestain M, Biggs PJ, Ganley ARD, O'Sullivan JM, McManus MT (2015) Biochar in co-contaminated soil manipulates arsenic solubility and microbiological community structure, and promotes organochlorine degradation. PLoS One 10(4):e0125393. https://doi.org/10.1371/journal.pone.0125393
Houben D, Evrard L, Sonnet P (2013) Beneficial effects of biochar application to contaminated soils on the bioavailability of Cd, Pb and Zn and the biomass production of rapeseed (Brassica napus L.) Biomass Bioenergy 57:196–204. https://doi.org/10.1016/j.biombioe.2013.07.019
Hu JL, Wu FY, Wu SC, Lam CL, Lin XG, Wong MH (2014) Biochar and glomus caledonium influence Cd accumulation of upland Kangkong (Ipomoea aquatica Forsk.) intercropped with Alfred stonecrop (Sedum alfredii Hance). Sci Rep 4:4671. https://doi.org/10.1038/srep04671
Inoue H, Fukuoka D, Tatai Y, Kamachi H, Hayatsu M, Ono M, Suzuki S (2013) Properties of lead deposits in cell walls of radish (Raphanus sativus) roots. J Plant Res 126(1):51–61
Inyang MI, Gao B, Yao Y, Xue YW, Zimmerman A, Mosa A, Pullammanappallil P, Ok YS, Cao XD (2016) A review of biochar as a low-cost adsorbent for aqueous heavy metal removal. Crit Rev Env Sci Tec 46(4):406–433. https://doi.org/10.1080/10643389.2015.1096880
Jaiswal AK, Elad Y, Paudel I, Graber ER, 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. Sci Rep 7:44382. https://doi.org/10.1038/srep44382
Javanbakht V, Alavi SA, Zilouei H (2014) Mechanisms of heavy metal removal using microorganisms as biosorbent. Water Sci Technol 69(9):1775–1787. https://doi.org/10.2166/wst.2013.718
Jeffery S, Verheijen FGA, van der Velde M, Bastos AC (2011) A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis. Agric Ecosyst Environ 144(1):175–187. https://doi.org/10.1016/j.agee.2011.08.015
Karami N, Clemente R, Moreno-Jimenez E, Lepp NW, Beesley L (2011) Efficiency of green waste compost and biochar soil amendments for reducing lead and copper mobility and uptake to ryegrass. J Hazard Mater 191(1-3):41–48. https://doi.org/10.1016/j.jhazmat.2011.04.025
Kumpiene J, Lagerkvist A, Maurice C (2008) Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments—a review. Waste Manag 28(1):215–225. https://doi.org/10.1016/j.wasman.2006.12.012
Laird DA, Fleming P, Davis DD, Horton R, Wang BQ, Karlen DL (2010) Impact of biochar amendments on the quality of a typical Midwestern agricultural soil. Geoderma 158(3-4):443–449. https://doi.org/10.1016/j.geoderma.2010.05.013
Lehmann J (2007) A handful of carbon. Nature 447(7141):143–144. https://doi.org/10.1038/447143a
Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota—a review. Soil Biol Biochem 43(9):1812–1836. https://doi.org/10.1016/j.soilbio.2011.04.022
Lentz RD, Ippolito JA (2012) Biochar and manure affect calcareous soil and corn silage nutrient concentrations and uptake. J Environ Qual 41(4):1033–1043. https://doi.org/10.2134/jeq2011.0126
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42(3):421–428. https://doi.org/10.2136/sssaj1978.03615995004200030009x
Lu KP, Yang X, Shen JJ, Robinson B, Huang HG, Liu D, Bolan N, Pei JC, Wang HL (2014) Effect of bamboo and rice straw biochars on the bioavailability of Cd, Cu, Pb and Zn to Sedum plumbizincicola. Agric Ecosyst Environ 191:124–132. https://doi.org/10.1016/j.agee.2014.04.010
Madiba OF, Solaiman ZM, Carson JK, Murphy DV (2016) Biochar increases availability and uptake of phosphorus to wheat under leaching conditions. Biol Fertil Soils 52(4):439–446. https://doi.org/10.1007/s00374-016-1099-3
Mulligan CN, Yong RN, Gibbs BF (2001) Remediation technologies for metal-contaminated soils and groundwater: an evaluation. Eng Geol 60(1-4):193–207. https://doi.org/10.1016/S0013-7952(00)00101-0
Nabavinia F, Emami H, Astaraee A, Lakzian A (2015) Effect of tannery wastes and biochar on soil chemical and physicochemical properties and growth traits of radish. Int Agrophys 29(3):333–339. https://doi.org/10.1515/intag-2015-0040
Namgay T, Singh B, Singh BP (2010) Influence of biochar application to soil on the availability of As, Cd, Cu, Pb, and Zn to maize (Zea mays L.) Aust J Soil Res 48(7):638–647. https://doi.org/10.1071/SR10049
Nguyen DH, Scheer C, Rowlings DW, Grace PR (2016) Rice husk biochar and crop residue amendment in subtropical cropping soils: effect on biomass production, nitrogen use efficiency and greenhouse gas emissions. Biol Fertil Soils 52(2):261–270. https://doi.org/10.1007/s00374-015-1074-4
Pahlsson AMB (1989) Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants. Water Air Soil Poll 47(3–4):287–319. https://doi.org/10.1007/BF00279329
Puga AP, Abreu CA, Melo LCA, Paz-Ferreiro J, Beesley L (2015) Cadmium, lead, and zinc mobility and plant uptake in a mine soil amended with sugarcane straw biochar. Environ Sci Pollut R 22(22):17606–17614. https://doi.org/10.1007/s11356-015-4977-6
Rieuwerts JS, Ashmore MR, Farago ME, Thornton I (2006) The influence of soil characteristics on the extractability of Cd, Pb and Zn in upland and moorland soils. Sci Total Environ 366(2-3):864–875. https://doi.org/10.1016/j.scitotenv.2005.08.023
Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4(10):1340–1351. https://doi.org/10.1038/ismej.2010.58
Rutigliano L, Fino D, Saracco G, Specchia V, Spinelli P (2008) Electrokinetic remediation of soils contaminated with heavy metals. J Appl Electrochem 38:1035–1041. https://doi.org/10.1007/s10800-008-9544-0
Tamaki H, Wright CL, Li XZ, Lin QY, Hwang CC, Wang SP, Thimmapuram J, Kamagata Y, Liu WT (2011) Analysis of 16S rRNA amplicon sequencing options on the roche/454 next-generation titanium sequencing platform. PLoS One 6(9):e25263. https://doi.org/10.1371/journal.pone.0025263
Tammeorg P, Simojoki A, Makela P, Stoddard FL, Alakukku L, Helenius J (2014) Short-term effects of biochar on soil properties and wheat yield formation with meat bone meal and inorganic fertiliser on a boreal loamy sand. Agric Ecosyst Environ 191:108–116. https://doi.org/10.1016/j.agee.2014.01.007
Teutscherova N, Vazquez E, Masaguer A, Navas M, Scow KM, Schmidt R, Benito M (2017) Comparison of lime- and biochar-mediated pH changes in nitrification and ammonia oxidizers in degraded acid soil. Biol Fertil Soils 53(7):811–821. https://doi.org/10.1007/s00374-017-1222-0
Tuberosa R (2012) Phenotyping for drought tolerance of crops in the genomics era. Front Physiol 3:347. https://doi.org/10.3389/fphys.2012.00347
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267. https://doi.org/10.1128/AEM.00062-07
Wang SJ, Chen HYH, Tan Y, Fan H, Ruan HH (2016) Fertilizer regime impacts on abundance and diversity of soil fauna across a poplar plantation chronosequence in coastal Eastern China. Sci Rep 6:20816. https://doi.org/10.1038/srep39807
Xie T, Reddy KR, Wang CW, Yargicoglu E, Spokas K (2015) Characteristics and applications of biochar for environmental remediation: a review. Crit Rev Env Sci Tec 45(9):939–969. https://doi.org/10.1080/10643389.2014.924180
Xu N, Tan GC, Wang HY, Gai XP (2016) Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Eur J Soil Biol 74:1–8. https://doi.org/10.1016/j.ejsobi.2016.02.004
Zhang ZH, Solaiman ZM, Meney K, Murphy DV, Rengel Z (2013) Biochars immobilize soil cadmium, but do not improve growth of emergent wetland species Juncus subsecundus in cadmium-contaminated soil. J Soils Sediment 13(1):140–151. https://doi.org/10.1007/s11368-012-0571-4
Zhang YY, Zhang SQ, Wang RZ, Cai JP, Zhang YG, Li H, Huang SM, Jiang Y (2016) Impacts of fertilization practices on pH and the pH buffering capacity of calcareous soil. Soil Sci Plant Nutr 62(5–6):432–439. https://doi.org/10.1080/00380768.2016.1226685
Zhang KL, Chen L, Li Y, Brookes PC, Xu JM, Luo Y (2017) The effects of combinations of biochar, lime, and organic fertilizer on nitrification and nitrifiers. Biol Fertil Soils 53(1):77–87. https://doi.org/10.1007/s00374-016-1154-0
Zheng RL, Cai C, Liang JH, Huang Q, Chen Z, Huang YZ, Arp HPH, Sun GX (2012) The effects of biochars from rice residue on the formation of iron plaque and the accumulation of Cd, Zn, Pb, As in rice (Oryza sativa L.) seedlings. Chemosphere 89(7):856–862. https://doi.org/10.1016/j.chemosphere.2012.05.008
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Nos. 41503080; 41773144), the Major S & T Special Project of Guizhou Province (No. [2014] 6015-2-1), the Key Technologies R & D Project in Agriculture of Guizhou Province (Nos. NY [2013] 3019; NY [2015] 3001-1), the “Thousand Talents Plan” of High-level Innovative Talents Cultivation Program of Guizhou Province (No. [2014] 122) and the National Natural Science Foundation of China (Grant No. U1612441). We also thank Editor-in-Chief Professor Paolo Nannipieri and three anonymous reviewers for their constructive comments and suggestions that improve the manuscript greatly and LetPub for improving English language.
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Cheng, J., Li, Y., Gao, W. et al. Effects of biochar on Cd and Pb mobility and microbial community composition in a calcareous soil planted with tobacco. Biol Fertil Soils 54, 373–383 (2018). https://doi.org/10.1007/s00374-018-1267-8
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DOI: https://doi.org/10.1007/s00374-018-1267-8