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Effects of biochar on copper immobilization and soil microbial communities in a metal-contaminated soil

  • Phytoremediation of Polluted Soils: Recent Progress and Developments
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Copper (Cu) contamination has been increasing in land ecosystems. Biochars (BCs) and arbuscular mycorrhizal fungi (AMF) are known to bind metals, and metallophyte can remove metals from soils. Will BC in combination with AMF contain the Cu uptake by a metallophyte growing in a metal-contaminated soil? The objective of this study was to investigate the effects of BCs on the Cu immobilization and over soil microbial communities in a metal-contaminated soil in the presence of AMF and metallophyte.

Materials and methods

Two BCs were produced from chicken manure (CMB) and oat hull (OHB). A Cu-contaminated sandy soil (338 mg kg−1) was incubated with CMB and OHB (0, 1, and 5 % w/w) for 2 weeks. Metallophyte Oenothera picensis was grown in pots (500 mL) containing the incubated soils in a controlled greenhouse for 6 months. A number of analyses were conducted after the harvest. These include plant biomass weight, microbial basal respiration, and dehydrogenase activity (DHA), AMF root colonization, spore number, and glomalin production; changes in fungal and bacterial communities, Cu fractions in soil phases, and Cu uptake in plant tissues.

Results and discussion

The BCs increased the soil pH, decreased easily exchangeable fraction of Cu, and increased organic matter and residual fraction of Cu. The BCs provided favorable habitat for microorganisms, thereby increasing basal respiration. The CMB increased DHA by ∼62 and ∼574 %, respectively, for the low and high doses. Similarly, the OHB increased soil microbial activity by ∼68 and ∼72 %, respectively, for the low and high doses. AMF root colonization, spore number, and total glomalin-related soil protein (GRSP) production increased by ∼3, ∼2, and ∼3 times, respectively, in soils treated with 1 % OHB. Despite being a metalophyte, O. picensis could not uptake Cu efficiently. Root and shoot Cu concentrations decreased or changed insignificantly in most BC treatments.

Conclusions

The results show that the BCs decreased bioavailable Cu, decreased Cu uptake by O. picensis, improved habitat for microorganisms, and enhanced plant growth in Cu-contaminated soil. This suggests that biochars may be utilized to remediate Cu-contaminated soils.

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References

  • Acuña JJ, Jorquera MA, Barra PJ, Crowley DE, de la Luz MM (2013) Selenobacteria selected from the rhizosphere as a potential tool for Se biofortification of wheat crops. Biol Fertil Soils 49:175–185

    Article  Google Scholar 

  • Anderson T, Domsch K (1990) Application of ecophysiological quotients (qCO2 and qD) on microbial biomasses from soils of different cropping histories. Soil Biol Biochem 22:251–255

    Article  Google Scholar 

  • Anderson CR, Condron LM, Clough TJ, Fiers M, Stewart A, Hill RA, Sherlock RR (2011) Biochar induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia (Jena) 54:309–320

    Article  CAS  Google Scholar 

  • Beesley L, Moreno-Jimenez E, Gomez-Eyles JL (2010) Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environ Pollut 158:2282–2287

    Article  CAS  Google Scholar 

  • Beesley L, Marmiroli M, Pagano L, Pigoni V, Fellet G, Fresno T, Vamerali T, Bandeira M, Marmiroli N (2013) Biochar addition to an arsenic contaminated soil increases arsenic concentrations in the pore water but reduces uptake to tomato plants (Solanum lycopersicum L.). Sci Total Environ 454–455:598–603

    Article  Google Scholar 

  • Belyaeva ON, Haynes RJ (2012) Comparison of the effects of conventional organic amendments and biochar on the chemical, physical and microbial properties of coal fly ash as a plant growth medium. Environ Earth Sci 66:1987–1997

    Article  CAS  Google Scholar 

  • Bloem J, Hopkins DW, Benedetti A (2006) Microbiological methods for assessing soil quality. Cabi Publishing, Wallingford, UK and Cambridge, USA

    Google Scholar 

  • Carrasco L, Caravaca F, Álvarez-Rogel J, Roldán A (2006) Microbial processes in the rhizosphere soil of a heavy metals-contaminated Mediterranean salt marsh: a facilitating role of AM fungi. Chemosphere 64:104–111

    Article  CAS  Google Scholar 

  • Cheng CH, Lehmann J, Engelhard MH (2008) Natural oxidation of black carbon in soils: changes in molecular form and surface charge along a climosequence. Geochim Cosmochim Acta 72:1598

    Article  CAS  Google Scholar 

  • Cornejo P, Pérez-Tienda J, Meier S, Valderas A, Borie F, Azcón-Aguilar C, Ferrol N (2013) Copper compartmentalization in spores as a survival strategy of arbuscular mycorrhizal fungi in Cu-polluted environments. Soil Biol Biochem 57:925–928

    Article  CAS  Google Scholar 

  • Gerdemann JW, Nicholson TH (1963) Spores of mycorrhizal endogene species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244

    Article  Google Scholar 

  • Ginocchio R, Carvallo G, Toro I, et al (2004) Micro-spatial variation of soil metal pollution and plant recruitment near a copper smelter in Central Chile. Environ Pollut 127:343–352. doi:10.1016/j.envpol.2003.08.020

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Gomez JD, Denef K, Stewart CE, Zheng J, Cotrufo MF (2014) Biochar addition rate influences soil microbial abundance and activity in temperate soils. Eur J Soil Sci 65:28–39

    Article  CAS  Google Scholar 

  • Haegeman B, Sen B, Godon JJ, Hamelin J (2014) Only Simpson diversity can be estimated accurately from microbial community fingerprints. Microb Ecol 68:169–172

    Article  Google Scholar 

  • Hsu N, Wang S, Lin Y, Sheng DG, Lee J (2009) Reduction of Cr (VI) by crop- residue-derived black carbon. Environ Sci Technol 43:8801–8806

    Article  CAS  Google Scholar 

  • Ippolito JA, Laird D, Busscher WJ (2012) Environmental benefits of biochar. J Environ Qual 41:967–972

    Article  CAS  Google Scholar 

  • Iwamoto T, Tani K, Nakamura K, Suzuki Y, Kitagawa M, Eguchi M, Nasu M (2000) Monitoring impact of in situ biostimulation treatment on groundwater bacterial community by DGGE. FEMS Microbiol Ecol 32:129–141

    Article  CAS  Google Scholar 

  • Johnson P, Sun N, Elimelech M (1996) Colloid transport in geochemically heterogeneous porous media: modeling and measurements. Environ Sci Technol 30:3284–3293

    Article  CAS  Google Scholar 

  • Karami N, Clemente R, Moreno-Jiménez 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 191:41–48

    Article  CAS  Google Scholar 

  • Khan AG (2006) Mycorrhizoremediation--an enhanced form of phytoremediation. J Zhejiang Univ Sci B 7:503–514

    Article  Google Scholar 

  • Khan N, Clark I, Sánchez-Monedero MA, Shea S, Meier S, Qi F, Kookana RS, Bolan N (2015) Physical and chemical properties of biochars co-composted with biowastes and incubated with a chicken litter compost. Chemosphere. doi:10.1016/j.chemosphere.2015.05.065

    Google Scholar 

  • Kookana RS, Sarmah AK, Van Zwieten L, Krull E, Singh B (2011) Biochar application to soil: agronomic and environmental benefits and unintended consequences. In: Donald LS (ed) Advances in agronomy, vol 112. Academic Press, pp 103–143

  • Lehmann J, Rillig MC, Thies J, Massiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota - a review. Soil Biol Biochem 43:1812–1836

    Article  CAS  Google Scholar 

  • Lu HL, Zhang WH, Yang YX, Huang X, Wang S, Qiu R (2012) Relative distribution of Pb2+ sorption mechanisms by sludge-derived biochar. Water Res 46:854–862

    Article  CAS  Google Scholar 

  • Lu H, Li Z, Fu S, Méndez A, Gascó G, Paz-Ferreiro J (2015) Combining phytoextraction and biochar addition improves soil biochemical properties in a soil contaminated with Cd. Chemosphere 119:209–216

    Article  CAS  Google Scholar 

  • Lucchini P, Quilliam RS, DeLuca TH, Vamerali T, Jones DL (2014) Does biochar application alter heavy metal dynamics in agricultural soil? Agric Ecosyst Environ 184:149–157

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282

    Article  CAS  Google Scholar 

  • Meier S, Azcón R, Cartes P, Borie F, Cornejo P (2011) Alleviation of Cu toxicity in Oenothera picensis by copper-adapted arbuscular mycorrhizal fungi and treated agrowaste residue. Appl Soil Ecol 48:117–124

    Article  Google Scholar 

  • Meier S, Alvear A, Borie F, Aguilera P, Ginocchio R, Cornejo P (2012a) Influence of copper on root exudate patterns in some metallophytes and agricultural plants. Ecotoxicol Environ Saf 75:8–15

    Article  CAS  Google Scholar 

  • Meier S, Borie F, Bolan N, Cornejo P (2012b) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42:741–775

    Article  CAS  Google Scholar 

  • Meier S, Borie F, Curaqueo G, Bolan N, Cornejo P (2012c) Effects of arbuscular mycorrhizal inoculation on metallophyte and agricultural plants growing at increasing copper levels. Appl Soil Ecol 61:280–287

    Article  Google Scholar 

  • Meier S, Cornejo P, Cartes P, Borie F, Medina J, Azcón R (2015) Interactive effect between Cu-adapted arbuscular mycorrhizal fungi and biotreated agrowaste residue to improve the nutritional status of Oenothera picensis growing in Cu-polluted soils. J Plant Nutr Soil Sci 178:126–135

    Article  CAS  Google Scholar 

  • Moreno-Castilla C, Lopez-Ramon M, Carrasco-Marín F (2000) Changes in surface chemistry of activated carbons by wet oxidation. Carbon N Y 38:1995–2001

    Article  CAS  Google Scholar 

  • Mulligan CN, Galvez-Cloutier R (2003) Bioremediation of metal contamination. Environ Monit Assess 84:45–60

    Article  CAS  Google Scholar 

  • Park JH, Choppala GK, Bolan NS, Chung JW, Chusavathi T (2011) Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant Soil 348:439–451

    Article  CAS  Google Scholar 

  • Pietikäinen J, Kiikkilä O, Fritze H (2000) Charcoal as a habitat for microbes and its effect on the microbial community of the underlying humus. Oikos 89:231–242

    Article  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Rutigliano FA, Romano M, Marzaioli R, Baglivo I, Baronti S, Miglietta F, Castaldi S (2014) Effect of biochar addition on soil microbial community in a wheat crop. Eur J Soil Biol 60:9–15

    Article  CAS  Google Scholar 

  • Sadzawka A, Carrasco MA, Grez R, et al (2006) Métodos de análisis recomendados para los suelos de Chile. Instituto de Investigaciones Agropecuarias. Santiago de Chile, Chile, 164 p

  • Schwitzguébel J-P (2001) Hype or hope: the potential of phytoremediation as an emerging green technology. Remediat J 11:63–78

    Article  Google Scholar 

  • Singh J, Singh D (2005) Dehydrogenase and phosphomonoenterase activities in groundnut (Arachis hypogacea L.) field after diazinon, imidacloprid and lindane treatments. Chemosphere 60:32–42

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, third. Academic Press, Amsterdam

    Google Scholar 

  • Tan KH (2005) Soil sampling, preparation, and analysis. CRC Press, Boca Raton

    Google Scholar 

  • Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851. doi:10.1021/ac50043a017

  • Wei L, Shutao W, Jin Z, Tong X (2014) Biochar influences the microbial community structure during tomato stalk composting with chicken manure. Bioresour Technol 154:148–154

    Article  Google Scholar 

  • Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107

    Article  CAS  Google Scholar 

  • Yang Y-J, Dungan R, Ibekwe AM, Valenzuela-Solano C, Crohn DM, Crowley DE (2003) Effect of organic mulches on soil bacterial communities one year after application. Biol Fertil Soils 38:273–281

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the postdoctoral Fondecyt project number 3130390, Universidad de La Frontera.

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Authors and Affiliations

  1. Scientifical and Technological Bioresource Nucleus, BIOREN-UFRO, Universidad de La Frontera, Box 54-D, Temuco, Chile

    Sebastián Meier, Gustavo Curaqueo, Joaquín Rilling, Catalina Vidal, Jacquelinne Acuña, Pablo Cornejo & Fernando Borie

  2. Centre for Environmental Risk Assessment and Remediation (CERAR), University of South Australia, Building X, University Blvd., Mawson Lakes, SA, 5095, Australia

    Naser Khan & Nanthi Bolan

  3. School of Natural and Built Environments, University of South Australia, Building P, Materials Lane, Mawson Lakes, SA, 5095, Australia

    Naser Khan & Nanthi Bolan

  4. Laboratorio de Microbiología Aplicada y Biotecnología, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue – INIBIOMA – CONICET, Quintral 1250, CP 8400, San Carlos de Bariloche, Argentina

    Natalia Fernández

  5. Núcleo de Investigación en Energías Renovables, Dirección de Investigación, Universidad Católica de Temuco, Temuco, Chile

    María-Eugenia González

Authors
  1. Sebastián Meier
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  2. Gustavo Curaqueo
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  7. Natalia Fernández
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  8. Jacquelinne Acuña
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  9. María-Eugenia González
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  10. Pablo Cornejo
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  11. Fernando Borie
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Correspondence to Sebastián Meier.

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Responsible editor: Zhenli He

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Meier, S., Curaqueo, G., Khan, N. et al. Effects of biochar on copper immobilization and soil microbial communities in a metal-contaminated soil. J Soils Sediments 17, 1237–1250 (2017). https://doi.org/10.1007/s11368-015-1224-1

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  • DOI: https://doi.org/10.1007/s11368-015-1224-1

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