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Environmental Science and Pollution Research

, Volume 25, Issue 23, pp 23106–23116 | Cite as

Evaluating the effects of phytoremediation with biochar additions on soil nitrogen mineralization enzymes and fungi

  • Manyun Zhang
  • Jun Wang
  • Shahla Hosseini Bai
  • Ying Teng
  • Zhihong Xu
Research Article
  • 224 Downloads

Abstract

Phytoremediation with biochar addition might alleviate pollutant toxicity to soil microorganism. It is uncertain to what extent biochar addition rate could affect activities of enzymes related to soil nitrogen (N) mineralization and alter fungal community under the phytoremediation. This study aimed to reveal the effects of Medicago sativa L. (alfalfa) phytoremediation, alone or with biochar additions, on soil protease and chitinase and fungal community and link the responses of microbial parameters with biochar addition rates. The alfalfa phytoremediation enhanced soil protease activities, and relative to the phytoremediation alone, biochar additions had inconsistent impacts on the corresponding functional gene abundances. Compared with the blank control, alfalfa phytoremediation, alone or with biochar additions, increased fungal biomass and community richness estimators. Moreover, relative to the phytoremediation alone, the relative abundances of phylum Zygomycota were also increased by biochar additions. The whole soil fungal community was not significantly changed by the alfalfa phytoremediation alone, but was indeed changed by alfalfa phytoremediation with 3.0% (w/w) or 6.0% biochar addition. This study suggested that alfalfa phytoremediation could enhance N mineralization enzyme activities and that biochar addition rates affected the responses of fungal community to the alfalfa phytoremediation.

Keywords

Medicago sativa L. Biochar Protease Chitinase Fungal biomass and community 

Notes

Acknowledgments

We sincerely thank the support from the Griffith University Ph.D. scholarships and from the Science Fund for Distinguished Young Scholars of Jiangsu Province, China (no. BK20150049).

Supplementary material

11356_2018_2425_MOESM1_ESM.docx (106 kb)
ESM 1 (DOCX 106 kb)

References

  1. Bach HJ, Hartmann A, Schloter M, Munch J (2001) PCR primers and functional probes for amplification and detection of bacterial genes for extracellular peptidases in single strains and in soil. J Microbiol Methods 44:173–182CrossRefGoogle Scholar
  2. Benny GL, Humber RA, Morton JB (2001) Zygomycota: zygomycetes. In: Systematics and evolution. Springer, Berlin, pp 113–146CrossRefGoogle Scholar
  3. Biederman LA, Harpole WS (2013) Biochar and its effects on plant productivity and nutrient cycling: a meta-analysis. GCB Bioenergy 5:202–214CrossRefGoogle Scholar
  4. Brockett BF, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44:9–20CrossRefGoogle Scholar
  5. Cajthaml T (2015) Biodegradation of endocrine-disrupting compounds by ligninolytic fungi: mechanisms involved in the degradation. Environ Microbiol 17:4822–4834CrossRefGoogle Scholar
  6. Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of Earth’s nitrogen cycle. Science 330:192–196CrossRefGoogle Scholar
  7. Cao X, Ma L, Gao B, Harris W (2009) Dairy-manure derived biochar effectively sorbs lead and atrazine. Environ Sci Technol 43:3285–3291CrossRefGoogle Scholar
  8. Chen J, Liu X, Zheng J, Zhang B, Lu H, Chi Z, Pan G, Li L, Zheng J, Zhang X (2013) Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from Southwest China. Appl Soil Ecol 71:33–44CrossRefGoogle Scholar
  9. De Vries FT, Hoffland E, van Eekeren N, Brussaard L, Bloem J (2006) Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol Biochem 38:2092–2103CrossRefGoogle Scholar
  10. Fernández-Calviño D, Arias-Estévez M, Díaz-Raviña M, Bååth E (2012) Assessing the effects of Cu and pH on microorganisms in highly acidic vineyard soils. Eur J Soil Sci 63:571–578CrossRefGoogle Scholar
  11. Ferraris M, Flora A, Chiesara E, Fornasari D, Lucchetti H, Marabini L, Frigerio S, Radice S (2005) Molecular mechanism of the aryl hydrocarbon receptor activation by the fungicide iprodione in rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 72:209–220CrossRefGoogle Scholar
  12. Geisseler D, Horwath WR (2008) Regulation of extracellular protease activity in soil in response to different sources and concentrations of nitrogen and carbon. Soil Biol Biochem 40:3040–3048CrossRefGoogle Scholar
  13. Geisseler D, Horwath WR, Joergensen RG, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms–a review. Soil Biol Biochem 42:2058–2067CrossRefGoogle Scholar
  14. Gianfreda L, Rao MA (2004) Potential of extra cellular enzymes in remediation of polluted soils: a review. Enzym Microb Technol 35:339–354CrossRefGoogle Scholar
  15. Hu L, Cao L, Zhang R (2014) Bacterial and fungal taxon changes in soil microbial community composition induced by short-term biochar amendment in red oxidized loam soil. World J Microb Biotechnol 30:1085–1092CrossRefGoogle Scholar
  16. Kepler RM, Ugine TA, Maul JE, Cavigelli MA, Rehner SA (2015) Community composition and population genetics of insect pathogenic fungi in the genus Metarhizium from soils of a long-term agricultural research system. Environ Microbiol 17:2791–2804CrossRefGoogle Scholar
  17. Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J (2008) Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8:2514–2530CrossRefGoogle Scholar
  18. Lazcano C, Gómez-Brandón M, Revilla P, Domínguez J (2013) Short-term effects of organic and inorganic fertilizers on soil microbial community structure and function. Biol Fertil Soils 49:723–733CrossRefGoogle Scholar
  19. Lebrun JD, Demont-Caulet N, Cheviron N, Laval K, Trinsoutrot-Gattin I, Mougin C (2016) Oxidoreductases provide a more generic response to metallic stressors (cu and cd) than hydrolases in soil fungi: new ecotoxicological insights. Environ Sci Pollut Res 23:3036–3041CrossRefGoogle Scholar
  20. Manzoni S, Jackson RB, Trofymow JA, Porporato A (2008) The global stoichiometry of litter nitrogen mineralization. Science 321:684–686CrossRefGoogle Scholar
  21. Neumann D, Heuer A, Hemkemeyer M, Martens R, Tebbe CC (2014) Importance of soil organic matter for the diversity of microorganisms involved in the degradation of organic pollutants. ISME J 8:1289–1300CrossRefGoogle Scholar
  22. Paz-Ferreiro J, Gascó G, Gutiérrez B, Méndez A (2012) Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil. Biol Fertil Soils 48:511–517CrossRefGoogle Scholar
  23. Qian L, Chen B, Hu D (2013) Effective alleviation of aluminum phytotoxicity by manure-derived biochar. Environ Sci Technol 47:2737–2745CrossRefGoogle Scholar
  24. Rai SK, Mukherjee AK (2009) Ecological significance and some biotechnological application of an organic solvent stable alkaline serine protease from Bacillus subtilis strain DM-04. Bioresour Technol 100:2642–2645CrossRefGoogle Scholar
  25. Ren W, Ren G, Teng Y, Li Z, Li L (2015) Time-dependent effect of graphene on the structure, abundance, and function of the soil bacterial community. J Hazard Mater 297:286–294CrossRefGoogle Scholar
  26. Rincón A, Santamaría-Pérez B, Rabasa SG, Coince A, Marçais B, Buée M (2015) Compartmentalized and contrasted response of ectomycorrhizal and soil fungal communities of Scots pine forests along elevation gradients in France and Spain. Environ Microbiol 17:3009–3024CrossRefGoogle Scholar
  27. Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596CrossRefGoogle Scholar
  28. Rousk J, Brookes PC, Bååth E (2010) Investigating the mechanisms for the opposing pH relationships of fungal and bacterial growth in soil. Soil Biol Biochem 42:926–934CrossRefGoogle Scholar
  29. Sopeña F, Bending GD (2013) Impacts of biochar on bioavailability of the fungicide azoxystrobin: a comparison of the effect on biodegradation rate and toxicity to the fungal community. Chemosphere 91:1525–1533CrossRefGoogle Scholar
  30. Sun Z, Bruun EW, Arthur E, de Jonge LW, Moldrup P, Hauggaard-Nielsen H, Elsgaard L (2014) Effect of biochar on aerobic processes, enzyme activity, and crop yields in two sandy loam soils. Biol Fertil Soils 50:1087–1097CrossRefGoogle Scholar
  31. Teng Y, Shen Y, Luo Y, Sun X, Sun M, Fu D, Li Z, Christie P (2011) Influence of Rhizobium meliloti on phytoremediation of polycyclic aromatic hydrocarbons by alfalfa in an aged contaminated soil. J Hazard Mater 186:1271–1276CrossRefGoogle Scholar
  32. Tian J, Wang J, Dippold M, Gao Y, Blagodatskaya E, Kuzyakov Y (2016) Biochar affects soil organic matter cycling and microbial functions but does not alter microbial community structure in a paddy soil. Sci Total Environ 556:89–97CrossRefGoogle Scholar
  33. Verchot LV, Borelli T (2005) Application of para-nitrophenol (pNP) enzyme assays in degraded tropical soils. Soil Biol Biochem 37:625–633CrossRefGoogle Scholar
  34. Wang X, Song Y, Ma Y, Zhuo R, Jin L (2011) Screening of Cd tolerant genotypes and isolation of metallothionein genes in alfalfa (Medicago sativa L.). Environ Pollut 159:3627–3633CrossRefGoogle Scholar
  35. Williams TD, Diab AM, George SG, Godfrey RE, Sabine V, Conesa A, Minchin SD, Watts PC, Chipman JK (2006) Development of the GENIPOL European flounder (Platichthys flesus) microarray and determination of temporal transcriptional responses to cadmium at low dose. Environ Sci Technol 40:6479–6488CrossRefGoogle Scholar
  36. Wu S, He H, Inthapanya X, Yang C, Lu L, Zeng G, Han Z (2017) Role of biochar on composting of organic wastes and remediation of contaminated soils-a review. Environ Sci Pollut Res 24:16560–16577CrossRefGoogle Scholar
  37. Xiao X, Yin X, Lin J, Sun L, You Z, Wang P, Wang F (2005) Chitinase genes in lake sediments of Ardley Island, Antarctica. Appl Environ Microbiol 71:7904–7909CrossRefGoogle Scholar
  38. Yao Q, Liu J, Yu Z, Li Y, Jin J, Liu X, Wang G (2017) Three years of biochar amendment alters soil physiochemical properties and fungal community composition in a black soil of northeast China. Soil Biol Biochem 110:56–67CrossRefGoogle Scholar
  39. Yasir M, Aslam Z, Kim SW, Lee S-W, Jeon CO, Chung YR (2009) Bacterial community composition and chitinase gene diversity of vermicompost with antifungal activity. Bioresour Technol 100:4396–4403CrossRefGoogle Scholar
  40. Zhang M, Bai SH, Tang L, Zhang Y, Teng Y, Xu Z (2017a) Linking potential nitrification rates, nitrogen cycling genes and soil properties after remediating the agricultural soil contaminated with heavy metal and fungicide. Chemosphere 184:892–899CrossRefGoogle Scholar
  41. Zhang M, Wang W, Wang J, Teng Y, Xu Z (2017b) Dynamics of biochemical properties associated with soil nitrogen mineralization following nitrification inhibitor and fungicide applications. Environ Sci Pollut Res 24:11340–11348CrossRefGoogle Scholar
  42. Zhang M, Bai SH, Zhang Y, Yang M, Teng Y, Xu Z (2018) Combined effects of Medicago sativa L and biochar on the remediation of soils co-contaminated by heavy metal and organic fungicide: pollutant removals and bacterial properties. Geoderma (Submitted)Google Scholar
  43. Zheng J, Chen J, Pan G, Liu X, Zhang X, Li L, Bian R, Cheng K, Jinwei Z (2016) Biochar decreased microbial metabolic quotient and shifted community composition four years after a single incorporation in a slightly acid rice paddy from southwest China. Sci Total Environ 571:206–217CrossRefGoogle Scholar
  44. Zhu X, Chen B, Zhu L, Xing B (2017) Effects and mechanisms of biochar-microbe interactions in soil improvement and pollution remediation: a review. Environ Pollut 227:98–115CrossRefGoogle Scholar
  45. Žifčáková L, Větrovský T, Howe A, Baldrian P (2016) Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol 18:288–301CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Environmental Futures Research Institute, School of Natural SciencesGriffith UniversityBrisbaneAustralia
  2. 2.Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil ScienceChinese Academy of SciencesNanjingChina
  3. 3.Chongqing Research Academy of Environmental SciencesChongqingChina
  4. 4.GeneCology Research Centre, Faculty of Science, Health, Education and EngineeringUniversity of the Sunshine CoastMaroochydore DCAustralia

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