Advertisement

Journal of Soils and Sediments

, Volume 20, Issue 1, pp 32–41 | Cite as

Influence of organic amendments used for benz[a]anthracene remediation in a farmland soil: pollutant distribution and bacterial changes

  • Qinghe Zhu
  • Yucheng Wu
  • Jun Zeng
  • Taolin Zhang
  • Xiangui LinEmail author
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • 92 Downloads

Abstract

Purpose

Organic amendments are usually carried out at field-scale for efficient remediation of organic pollutants; however, their effects on pollutant distribution and the corresponding microbial mechanisms were rarely discussed. The main aim of this study was to compare the fate of benz[a]anthracene in soil amended by several bioremediation materials and underlying microbial mechanisms.

Materials and methods

In this study, the potential for biotransformation of polycyclic aromatic hydrocarbon in a farmland soil was investigated in microcosms spiked with 14C-benz[a]anthracene as the tracer. A series of organic amendments including lignin, straw, mushroom culture waste, and cow manure, as well as a fungal inoculum of Pleurotus ostreatus, were compared. Illumina sequencing was introduced to reveal the bacterial community in different amendments. The metagenomic function was predicted with the bioinformatics tool of phylogenetic investigation of communities by reconstruction of unobserved states (PICRUSt).

Results and discussion

From the results, the lignin-contained substrates (lignin, straw, mushroom culture waste) showed increase trend in the dissipation of benz[a]anthracene, while Pleurotus ostreatus and cow manure resulted in opposite trends. Specifically, mushroom culture waste mainly increased 14C to the formation of humin-bound residue (39.5 ± 6.8%); lignin amendment significantly (P < 0.05) enhanced the mineralization to CO2 (7.38 ± 0.89%) and humic acid–related nonextractable residue (9.77 ± 0.45%). The influence of straw on the environmental fate of benz[a]anthracene was marginal. High-throughput sequencing of 16S rRNA genes demonstrated that mushroom culture waste and lignin significantly changed bacterial community composition, leading to increases in the relative abundance of Pseudomonadaceae, Methylophilaceae, Bacillaceae, and Burkholderiaceae. Moreover, the result of PICRUSt showed that the genes-encoding bacterial cytochrome P450 enzymes were significantly increased in the lignin treatment, suggesting a possible co-metabolism between lignin degradation and PAH mineralization.

Conclusions

These findings suggest lignin-containing organic amendments could be promising soil remediation agents of benz[a]anthracene by stimulating mineralization and sequestration of pollutants.

Keywords

Bioremediation Bound residue C-14-Benz[a]anthracene Mineralization 

Notes

Funding information

We thank Professor Ji Rong and his group for the help with the isotopic analysis. This work was supported the National Natural Science Foundation of China (41371310, 41671266) and the Natural Science Foundation of Jiangsu Province (BK20181512).

Compliance with ethical standards

Conflict of interest

The authors declared that they have no conflict of interest.

Supplementary material

11368_2019_2368_MOESM1_ESM.docx (6 mb)
ESM 1 (DOCX 5.96 mb)

References

  1. Adam IKU, Miltner A, Kastner M (2015) Degradation of C-13-labeled pyrene in soil-compost mixtures and fertilized soil. Appl Microbiol Biot 99:9813–9824Google Scholar
  2. Alvarez-Bernal D, Garcıa-Dıaz EL, Contreras-Ramos SM, Dendooven L (2006) Dissipation of polycyclic aromatic hydrocarbons from soil added with manure or vermicompost. Chemosphere 65:1642–1651Google Scholar
  3. Amalfitano C, Pignalosa V, Auriemma L, Uriemma L, Ramunni A (1992) The contribution of lignin to the composition of humic acid from a wheat-straw amended soil during 3 years of incubation in pots. J Soil Sci 43:495–504Google Scholar
  4. Brezna B, Kweon O, Stingley RL, Freeman JP, Khan AA, Polek B, Jones RC, Cerniglia CE (2006) Molecular characterization of cytochrome P450 genes in the polycyclic aromatic hydrocarbon degrading Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biotechnol 71:522–532Google Scholar
  5. Cajthmal T, Erbanova P, Sasek V, Moeder M (2006) Breakdown products on metabolic pathway of degradation of benz[a]anthracene by a ligninolytic fungus. Chemosphere 64:560–564Google Scholar
  6. Cebron A, Norini MP, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHD alpha) genes from gram positive and gram negative bacteria in soil and sediment samples. J Microbiol Meth 73:148–159Google Scholar
  7. Cebron A, Beguiristain T, Bongoua-Devisme J, Denonfoux J, Faure P, Lorgeoux C, Ouvrard S, Parisot N, Peyret P, Leyval C (2015) Impact of clay mineral, wood sawdust or root organic matter on the bacterial and fungal community structures in two aged PAH-contaminated soils. Environ Sci Pollut Res 22:13724–13738Google Scholar
  8. Chaignaud P, Morawe M, Besaury L, Kroeber E, Vuilleumier S, Bringel F, Kolb S (2018) Methanol consumption drives the bacterial choromethane sink in a forest soil. ISME J 12:2681–2693Google Scholar
  9. Chemerys A, Pelletier E, Cruaud C, Martin F, Violet F, Jouanneau Y (2014) Characterization of novel polycyclic aromatic hydrocarbon dioxygenases from the bacterial metagenomic DNA of a contaminated soil. Appl Environ Microbiol 80:6591–6600Google Scholar
  10. Crampon M, Bodilisb J, Portet-Koltalo F (2018) Linking initial soil bacterial diversity and polycyclic aromatic hydrocarbons (PAHs) degradation potential. J Hazard Mater 359:500–509Google Scholar
  11. Doick KJ, Lee PH, Semple KT (2003) Assessment of spiking procedures for the introduction of a phenanthrene-LNAPL mixture into field-wet soil. Environ Pollut 126:399–406Google Scholar
  12. Du WC, Sun YY, Cao L, Huang J, Ji R, Wang XR, Wu JC, Zhu JG, Guo HY (2011) Environmental fate of phenanthrene in lysimeter planted with wheat and rice in rotation. J Hazard Mater 188:408–413Google Scholar
  13. Gao BQ, Li P, Yang R, Li AM, Yang H (2019) Investigation of multiple adsorption mechanisms for efficient removal of ofloxacin from water using lignin-based adsorbents. Sci Rep 9:637Google Scholar
  14. Garcia-Delgado C, D'Annibale A, Pesciaroli L, Yunta F, Crognale S, Petruccioli M, Eymar E (2015) Implications of polluted soil biostimulation and bioaugmentation with spent mushroom substrate (Agaricus bisporus) on the microbial community and polycyclic aromatic hydrocarbons biodegradation. Sci Total Environ 508:20–28Google Scholar
  15. Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369Google Scholar
  16. Gu JQ, Zhou WQ, Jiang BQ, Wang LH, Ma YN, Guo HY, Schulin R, Ji R, Evangelou MWH (2016) Effects of biochar on the transformation and earthworm bioaccumulation of organic pollutants in soil. Chemosphere 145:431–437Google Scholar
  17. Guntupalli S, Thunuguntla VBSC, Chalasani LM, Rao CV, Bondili JS (2019) Degradation and metabolite profiling of benz[a]anthracene, dibenz(a, h)anthracene and indeno[1, 2, 3-cd]pyrene by Aspergillus terricola. Polycycl Aromat Comp 39:84–92Google Scholar
  18. Guo XX, Liu HT, Wu SB (2019) Humic substances developed during organic waste composting: formation mechanisms, structural properties, and agronomic functions. Sci Total Environ 662:501–510Google Scholar
  19. Hamdi H, Benzarti S, Manusadžianas L, Aoyama I, Jedidid N (2007) Bioaugmentation and biostimulation effects on PAH dissipation and soil ecotoxicity under controlled conditions. Soil Biol Biochem 39:1926–1935Google Scholar
  20. Han XM, Hu HW, Shi XZ, Zhang LM, He JZ (2017) Effects of different agricultural wastes on the dissipation of PAHs and the PAH degrading genes in a PAH-contaminated soil. Chemosphere 172:286–293Google Scholar
  21. Holman HYN, Nieman K, Sorensen DL, Miller CD, Martin MC, Borch T, Mckinney WR, Sims RC (2002) Catalysis of PAH biodegradation by humic acid shown in synchrotron infrared studies. Environ Sci Technol 36:1276–1280Google Scholar
  22. Juhasz AL, Britz ML, Stanley GA (1997) Degradation of fluoranthene, pyrene, benz[a]anthracene and dibenz[a,h]anthracene by Burkholderia cepacia. J Appl Microbiol 83:189–198Google Scholar
  23. Kästner M, Nowak KM, Miltner A, Trapp S, Schäffer A (2014) Classification and modelling of non-extractable residue (NER) formation of xenobiotics in soil – a synthesis. Crit Rev Environ Sci Technol 44:2107–2171Google Scholar
  24. Kästner M, Nowak KM, Miltner A, Schaffer A (2016) (multiple) isotope probing approaches to trace the fate of environmental chemicals and the formation of non-extractable 'bound' residues. Curr Opin Biotech 41:73–82Google Scholar
  25. Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638Google Scholar
  26. Kunihiro M, Ozeki Y, Nogi Y, Hamamura N, Kanaly RA (2013) Benz[a]anthracene biotransformation and production of ring fission products by Sphingobium sp. strain KK22. Appl Environ Microb 79:14Google Scholar
  27. Li XZ, Wu YC, Lin XG, Zhang J, Zeng J (2012) Dissipation of polycyclic aromatic hydrocarbons (PAHs) in soil microcosms amended with mushroom cultivation substrate. Soil Biol Biochem 47:191–197Google Scholar
  28. Li JB, Zhang DY, Song MK, Jiang LF, Wang YJ, Luo CL, Zhang G (2017) Novel bacteria capable of degrading phenanthrene in activated sludge revealed by stable-isotope probing coupled with high-throughput sequencing. Biodegradation 28:423–436Google Scholar
  29. Lladó S, Covino S, Solanas AM, Vinas M, Petruccioli M, D’annibale A (2013) Comparative assessment of bioremediation approaches to highly recalcitrant PAH degradation in a real industrial polluted soil. J Hazard Mater 248-249:407–414Google Scholar
  30. Longe LF, Couvreur J, Grandchamp ML, Garnier G, Allais F, Saito K (2018) Importance of mediators for lignin degradation by fungal laccase. ACS Sustain Chem Eng 6:10097–10107Google Scholar
  31. Luo Y, Hui D, Zhang D (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63Google Scholar
  32. Luo A, Wu YR, Xu Y, Kan J, Qiao J, Liang L, Huang TW, Hu Z (2016) Characterization of a cytochrome P450 monooxygenase capable of high molecular weight PAHs oxidization from Rhodococcus sp. P14. Process Biochem 51:2127–2133Google Scholar
  33. Mallinson SJB, Machovina MM, Silveira RL, Garcia-Borras M, Gallup N, Johnson CW, Allen MD, Skaf MS, Crowley MF, Neidle EL, Houk KN, Beckham GT, DuBois JL, McGeehan JE (2018) A promiscuous cytochrome P450 aromatic O-demethylase for lignin bioconversion. Nat Commun 9:2487Google Scholar
  34. Moody JD, Freeman JP, Fu PP, Cerniglia CE (2004) Degradation of benzo[a]pyrene by Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 70:340–345Google Scholar
  35. Nisbet ICT, Lagoy PK (1992) Toxic equivalency factors (TEFs) for polycyclic aromatic hydrocarbons (PAHs). Regul Toxicol Pharmacol 16:290–300Google Scholar
  36. Novotny C, Svobodova K, Erbanova P, Cajthaml T, Kasinath A, Lang E, Sasek V (2004) Ligninolytic fungi in bioremediation: extracellular enzyme production and degradation rate. Soil Biol Biochem 36:1545–1551Google Scholar
  37. Nowak KM, Miltner A, Gehre M, Schaffer A, Kastner M (2011) Formation and fate of bound residues from microbial biomass during 2,4-D degradation in soil. Environ Sci Technol 45:999–1006Google Scholar
  38. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Package ‘vegan’. Community Ecology Package, Version 2Google Scholar
  39. Oyehan TA, Al-Thukair AA (2017) Isolation and characterization of PAH-degrading bacteria from the Eastern Province, Saudi Arabia. Mar Pollut Bull 115:39–46Google Scholar
  40. Peng T, Luo A, Kan J, Liang L, Huang TW, Hu Z (2018) Identification of a ring-hydroxylating dioxygenases capable of anthracene and benz[a]anthracene oxidization from Rhodococcus sp. P14. J Mol Microb Biotech 28:183–189Google Scholar
  41. Satapute P, Kaliwal B (2016) Biodegradation of the fungicide propiconazole by Pseudomonas aeruginosa PS-4 strain isolated from a paddy soil. Ann Microbiol 66:1355–1365Google Scholar
  42. Schmidt S, Christensen J, Johnsen A (2010) Fungal PAH-metabolites resist mineralization by soil microorganisms. Environ Sci Technol 44:1677–1682Google Scholar
  43. Semrau JD (2011) Bioremediation via methanotrophy: overview of recent findings and suggestions for future research. Front Microbiol 2:209Google Scholar
  44. Shan J, Jiang B, Yu B, Li C, Sun Y, Guo H, Wu J, Klumpp E, Schäffer A, Ji R (2011) Isomer-specific degradation of branched and linear 4-nonylphenol isomers in an oxic soil. Environ Sci Technol 45:8283–8289Google Scholar
  45. Singh CP, Amberger A (1990) Humic substances in straw compost with rock phosphate. Biol Wastes 31:165–174Google Scholar
  46. Syed K, Porollo A, Lam YW, Grimmett PE, Yadav JS (2013) CYP63A2, a catalytically versatile fungal P450 monooxygenase capable of oxidizing higher-molecular-weight polycyclic aromatic hydrocarbons, alkylphenols, and alkanes. Appl Environ Microbiol 79:2692–2702Google Scholar
  47. Tang B, Lei P, Xu ZQ, Jiang YX, Xu Z, Liang JF, Feng XH, Xu H (2015) Highly efficient rice straw utilization for poly-(gamma-glutamic acid) production by Bacillus subtilis NX-2. Bioresour Technol 193:370–376Google Scholar
  48. Tejeda-Agredano M, Mayer P, Ortega-Calvo J (2014) The effect of humic acids on biodegradation of polycyclic aromatic hydrocarbons depends on the exposure regime. Environ Pollut 184:435–442Google Scholar
  49. van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci U S A 109(4):1159–1164Google Scholar
  50. Wu YC, Teng Y, Li ZG, Liao XW, Luo YM (2008) Potential role of polycyclic aromatic hydrocarbons (PAHs) oxidation by fungal laccase in the remediation of an aged contaminated soil. Soil Biol Biochem 40:789–796Google Scholar
  51. Wu YR, Luo ZH, Vrijmoed LLP (2010) Biodegradation of anthracene and benz[a]anthracene by two Fusarium solani strains isolated from mangrove sediments. Bioresource Tech 101:9666–9672Google Scholar
  52. Wu GZ, Kechavarzi C, Li XG, Sui H, Pollard SJT, Coulon F (2013) Influence of mature compost amendment on total and bioavailable polycyclic aromatic hydrocarbons in contaminated soils. Chemosphere 90:2240–2246Google Scholar
  53. Wu YC, Ding QM, Zhu QH, Zeng J, Ji R, Dumont MG, Lin XG (2018) Contributions of ryegrass, lignin and rhamnolipid to polycyclic aromatic hydrocarbon dissipation in an arable soil. Soil Biol Biochem 118:27–34Google Scholar
  54. Xi ZM, Chen BL (2014) Removal of polycyclic aromatic hydrocarbons from aqueous solution by raw and modified plant residue materials as biosorbents. J Environ Sci 26:737–748Google Scholar
  55. Xu YH, Lu M (2010) Bioremediation of crude oil-contaminated soil: comparison of different biostimulation and bioaugmentation treatments. J Hazard Mater 183:395–401Google Scholar
  56. Zafa G, Taylor TD, Absalón AE, Cortés-Espinosa DV (2016) Comparative metagenomic analysis of PAH degradation in soil by a mixed microbial consortium. J Hazard Mater 318:702–710Google Scholar
  57. Zeng J, Zhu QH, Wu YC, Lin XG (2016) Oxidation of polycyclic aromatic hydrocarbons using Bacillus subtilis CotA with high laccase activity and copper independence. Chemosphere 148:1–7Google Scholar
  58. Zeng J, Zhu QH, Wu YC, Shan J, Ji R, Lin XG (2018) Oxidation of benzo[a]pyrene by laccase in soil enhances bound residue formation and reduces disturbance to soil bacterial community composition. Environ Pollut 242:462–469Google Scholar
  59. Zhang YX, Tao S, Cao J, Coveney RM (2007) Emission of polycyclic aromatic hydrocarbons in China by country. Environ Sci Technol 41:683–687Google Scholar
  60. Zhang K, Hua XF, Han HL, Wang J, Miao CC, Xu YY, Huang ZD, Zhang H, Yang JM, Jin WB, Liu YM, Liu Z (2008) Enhanced bioaugmentation of petroleum- and salt-contaminated soil using wheat straw. Chemosphere 73:1387–1392Google Scholar
  61. Zhu QH, Wu YC, Zeng J, Wang XX, Zhang TL, Lin XG (2019) Influence of bacterial community composition and soil factors on the fate of phenanthrene and benzo[a]pyrene in three contrasting farmland soils. Environ Pollut 247:229–237Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil ScienceChinese Academy of SciencesNanjingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations