Skip to main content
SpringerLink
Log in

Microbial remediation of aromatics-contaminated soil

  • Feature Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

Aromatics-contaminated soil is of particular environmental concern as it exhibits carcinogenic and mutagenic properties. Bioremediation, a biological approach for the removal of soil contaminants, has several advantages over traditional soil remediation methodologies including high efficiency, complete pollutant removal, low expense and limited or no secondary pollution. Bioaugmentation, defined as the introduction of specific competent strains or consortia of microorganisms, is a widely applied bioremediation technology for soil remediation. In this review, it is concluded which several successful studies of bioaugmentation of aromatics-contaminated soil by single strains or mixed consortia. In recent decades, a number of reports have been published on the metabolic machinery of aromatics degradation by microorganisms and their capacity to adapt to aromatics-contaminated environments. Thus, microorganisms are major players in site remediation. The bioremediation/bioaugmentation process relies on the immense metabolic capacities of microbes for transformation of aromatic pollutants into essentially harmless or, at least, less toxic compounds. Aromatics-contaminated soils are successfully remediated with adding not only single strains but also bacterial or fungal consortia. Furthermore several novel approaches, which microbes combined with physical, chemical or biological factors, increase remediation efficiency of aromatics-contaminated soil. Meanwhile, the environmental factors also have appreciable impacts on the bioaugmentation process. The biostatistics method is recommended for analysis of the effects of bioaugmentation treatments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. O’Neil M J, Heckelman P E, Dobbelaar P H, Roman K J, Kenny C M, Karaffa L S. The Merck Index: An Encyclopedia of Chemicals, Drugs, and Biologicals. 15th ed. London: The Royal Society of Chemistry, 2013

    Google Scholar 

  2. Toyoshima E, Mayer R F, Max S R, Eccles C. 2,4-Dichlorophenoxyacetic acid (2,4-D) does not cause polyneuropathy in the rat. Journal of the Neurological Sciences, 1985, 70(2): 225–229

    Article  CAS  Google Scholar 

  3. Xiao Y, Zhang J J, Liu H, Zhou N Y. Molecular characterization of a novel ortho-nitrophenol catabolic gene cluster in Alcaligenes sp. strain NyZ215. Journal of Bacteriology, 2007, 189(18): 6587–6593

    Article  CAS  Google Scholar 

  4. Zhang J J, Liu H, Xiao Y, Zhang X E, Zhou N Y. Identification and characterization of catabolic para-nitrophenol 4-monooxygenase and para-benzoquinone reductase from Pseudomonas sp. strain WBC-3. Journal of Bacteriology, 2009, 191(8): 2703–2710

    Article  CAS  Google Scholar 

  5. Zhen D, Liu H, Wang S J, Zhang J J, Zhao F, Zhou N Y. Plasmidmediated degradation of 4-chloronitrobenzene by newly isolated Pseudomonas putida strain ZWL73. Applied Microbiology and Biotechnology, 2006, 72(4): 797–803

    Article  CAS  Google Scholar 

  6. Yin Y, Xiao Y, Liu H Z, Hao F, Rayner S, Tang H, Zhou N Y. Characterization of catabolic meta-nitrophenol nitroreductase from Cupriavidus necator JMP134. Applied Microbiology and Biotechnology, 2010, 87(6): 2077–2085

    Article  CAS  Google Scholar 

  7. Pérez-Pantoja D, De la Iglesia R, Pieper D H, González B. Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiology Reviews, 2008, 32(5): 736–794

    Article  Google Scholar 

  8. Shen X H, Zhou N Y, Liu S J. Degradation and assimilation of aromatic compounds by Corynebacterium glutamicum: another potential for applications for this bacterium? Applied Microbiology and Biotechnology, 2012, 95(1): 77–89

    Article  CAS  Google Scholar 

  9. Liu H, Wang S J, Zhang J J, Dai H, Tang H, Zhou N Y. Patchwork assembly of nag-like nitroarene dioxygenase genes and the 3- chlorocatechol degradation cluster for evolution of the 2-chloronitrobenzene catabolism pathway in Pseudomonas stutzeri ZWLR2-1. Applied and Environmental Microbiology, 2011, 77(13): 4547–4552

    Article  CAS  Google Scholar 

  10. Min J, Zhang J J, Zhou N Y. A two-component para-nitrophenol monooxygenase initiates a novel 2-chloro-4-nitrophenol catabolism pathway in Rhodococcus imtechensis RKJ300. Applied and Environmental Microbiology, 2016, 82(2): 714–723

    Article  CAS  Google Scholar 

  11. Chao H J, Chen Y F, Fang T, Xu Y, Huang W E, Zhou N Y. HipH catalyzes the hydroxylation of 4-hydroxyisophthalate to protocatechuate in 2,4-xylenol catabolism by Pseudomonas putida NCIMB 9866. Applied and Environmental Microbiology, 2016, 82(2): 724–731

    Article  CAS  Google Scholar 

  12. Azubuike C C, Chikere C B, Okpokwasili G C. Bioremediation techniques–classification based on site of application: principles, advantages, limitations and prospects. World Journal of Microbiology and Biotechnology, 2016, 32(11): 180

    Article  Google Scholar 

  13. El Fantroussi S, Agathos S N. Is bioaugmentation a feasible strategy for pollutant removal and site remediation? Current Opinion in Microbiology, 2005, 8(3): 268–275

    Article  CAS  Google Scholar 

  14. Dechesne A, Pallud C, Bertolla F, Grundmann G L. Impact of the microscale distribution of a Pseudomonas strain introduced into soil on potential contacts with indigenous bacteria. Applied and Environmental Microbiology, 2005, 71(12): 8123–8131

    Article  CAS  Google Scholar 

  15. Martín-Hernández M, Suárez-Ojeda M E, Carrera J. Bioaugmentation for treating transient or continuous p-nitrophenol shock loads in an aerobic sequencing batch reactor. Bioresource Technology, 2012, 123: 150–156

    Article  Google Scholar 

  16. Vogel T M. Bioaugmentation as a soil bioremediation approach. Current Opinion in Biotechnology, 1996, 7(3): 311–316

    Article  CAS  Google Scholar 

  17. Jasper D A. Bioremediation of agricultural and forestry soils with symbiotic micro-organisms. Soil Research, 1994, 32(6): 1301–1319

    Article  Google Scholar 

  18. Menashe O, Kurzbaum E. A novel bioaugmentation treatment approach using a confined microbial environment: a case study in a Membrane Bioreactor wastewater treatment plant. Environmental Technology, 37(12): 1–23

  19. Chi X Q, Zhang J J, Zhao S, Zhou N Y. Bioaugmentation with a consortium of bacterial nitrophenol-degraders for remediation of soil contaminated with three nitrophenol isomers. Environmental Pollution, 2013, 172: 33–41

    Article  CAS  Google Scholar 

  20. Wang L M, Chi X Q, Zhang J J, Sun D L, Zhou N Y. Bioaugmentation of a methyl parathion contaminated soil with Pseudomonas sp strain WBC-3. International Biodeterioration & Biodegradation, 2014, 87(1): 116–121

    Article  CAS  Google Scholar 

  21. Zhao S, Ramette A, Niu G L, Liu H, Zhou N Y. Effects of nitrobenzene contamination and of bioaugmentation on nitrification and ammonia-oxidizing bacteria in soil. FEMS Microbiology Ecology, 2009, 70(2): 315–323

    Article  CAS  Google Scholar 

  22. Niu G L, Zhang J J, Zhao S, Liu H, Boon N, Zhou N Y. Bioaugmentation of a 4-chloronitrobenzene contaminated soil with Pseudomonas putida ZWL73. Environmental Pollution, 2009, 157(3): 763–771

    Article  CAS  Google Scholar 

  23. Liu L, Jiang C Y, Liu X Y, Wu J F, Han J G, Liu S J. Plant-microbe association for rhizoremediation of chloronitroaromatic pollutants with Comamonas sp. strain CNB-1. Environmental Microbiology, 2007, 9(2): 465–473

    Article  CAS  Google Scholar 

  24. Hong Q, Zhang Z H, Hong Y F, Li S. A microcosm study on bioremediation of fenitrothion-contaminated soil using Burkholderia sp. FDS-1. International Biodeterioration & Biodegradation, 2007, 59(1): 55–61

    Article  CAS  Google Scholar 

  25. Dams R I, Paton G, Killham K. Bioaugmentation of pentachlorophenol in soil and hydroponic systems. International Biodeterioration & Biodegradation, 2007, 60(3): 171–177

    Article  CAS  Google Scholar 

  26. Qiao J, Zhang C D, Luo SM, Chen W. Bioremediation of highly contaminated oilfield soil: bioaugmentation for enhancing aromatic compounds removal. Frontiers of Environmental Science & Engineering, 2014, 8(2): 293–304

    Article  CAS  Google Scholar 

  27. Xu W D, Guo S H, Li G, Li F M, Wu B, Gan X H. Combination of the direct electro-Fenton process and bioremediation for the treatment of pyrene-contaminated soil in a slurry reactor. Frontiers of Environmental Science & Engineering, 2015, 9(6): 1096–1107

    Article  CAS  Google Scholar 

  28. Jézéquel K, Lebeau T. Soil bioaugmentation by free and immobilized bacteria to reduce potentially phytoavailable cadmium. Bioresource Technology, 2008, 99(4): 690–698

    Article  Google Scholar 

  29. Beolchini F, Dell’Anno A, De Propris L, Ubaldini S, Cerrone F, Danovaro R. Auto- and heterotrophic acidophilic bacteria enhance the bioremediation efficiency of sediments contaminated by heavy metals. Chemosphere, 2009, 74(10): 1321–1326

    Article  CAS  Google Scholar 

  30. Lebeau T, Braud A, Jézéquel K. Performance of bioaugmentationassisted phytoextraction applied to metal contaminated soils: a review. Environmental Pollution, 2008, 153(3): 497–522

    Article  CAS  Google Scholar 

  31. Gavrilescu M, Pavel L V, Cretescu I. Characterization and remediation of soils contaminated with uranium. Journal of Hazardous Materials, 2009, 163(2–3): 475–510

    Article  CAS  Google Scholar 

  32. Kumar R, Singh S, Singh O V. Bioremediation of radionuclides: emerging technologies. OMICS: A Journal of Integrative Biology, 2007, 11(3): 295–304

    Article  CAS  Google Scholar 

  33. Sun Y B, Zhao D, Xu Y M, Wang L, Liang X F, Shen Y. Effects of sepiolite on stabilization remediation of heavy metal-contaminated soil and its ecological evaluation. Frontiers of Environmental Science & Engineering, 2016, 10(1): 85–92

    Article  CAS  Google Scholar 

  34. Xiao Y, Wu J F, Liu H, Wang S J, Liu S J, Zhou N Y. Characterization of genes involved in the initial reactions of 4- chloronitrobenzene degradation in Pseudomonas putida ZWL73. Applied Microbiology and Biotechnology, 2006, 73(1): 166–171

    Article  CAS  Google Scholar 

  35. Zhang Z H, Hong Q, Xu J H, Zhang X, Li S. Isolation of fenitrothion-degrading strain Burkholderia sp. FDS-1 and cloning of mpd gene. Biodegradation, 2006, 17(3): 275–283

    Article  CAS  Google Scholar 

  36. Jain R K, Dreisbach J H, Spain J C. Biodegradation of p-nitrophenol via 1,2,4-benzenetriol by an Arthrobacter sp. Applied and Environmental Microbiology, 1994, 60(8): 3030–3032

    CAS  Google Scholar 

  37. Kadiyala V, Spain J C. A two-component monooxygenase catalyzes both the hydroxylation of p-nitrophenol and the oxidative release of nitrite from 4-nitrocatechol in Bacillus sphaericus JS905. Applied and Environmental Microbiology, 1998, 64(7): 2479–2484

    CAS  Google Scholar 

  38. Spain J C, Gibson D T. Pathway for Biodegradation of p-Nitrophenol in a Moraxella sp. Applied and Environmental Microbiology, 1991, 57(3): 812–819

    CAS  Google Scholar 

  39. Labana S, Pandey G, Paul D, Sharma N K, Basu A, Jain R K. Pot and field studies on bioremediation of p-nitrophenol contaminated soil using Arthrobacter protophormiae RKJ100. Environmental Science & Technology, 2005, 39(9): 3330–3337

    Article  CAS  Google Scholar 

  40. Liu H, Zhang J J, Wang S J, Zhang X E, Zhou N Y. Plasmid-borne catabolism of methyl parathion and p-nitrophenol in Pseudomonas sp. strain WBC-3. Biochemical and Biophysical Research Communications, 2005, 334(4): 1107–1114

    Article  CAS  Google Scholar 

  41. Middaugh D P, Thomas R L, Lantz S E, Heard C S, Mueller J G. Field scale testing of a hyperfiltration unit for removal of creosote and pentachlorophenol from ground water: chemical and biological assessment. Archives of Environmental Contamination and Toxicology, 1994, 26(3): 309–319

    CAS  Google Scholar 

  42. Cai M, Xun L. Organization and regulation of pentachlorophenoldegrading genes in Sphingobium chlorophenolicum ATCC 39723. Journal of Bacteriology, 2002, 184(17): 4672–4680

    Article  CAS  Google Scholar 

  43. Dams R I, Paton G I, Killham K. Rhizoremediation of pentachlorophenol by Sphingobium chlorophenolicum ATCC 39723. Chemosphere, 2007, 68(5): 864–870

    Article  CAS  Google Scholar 

  44. Jernberg C, Jansson J K. Impact of 4-chlorophenol contamination and/or inoculation with the 4-chlorophenol-degrading strain, Arthrobacter chlorophenolicus A6L, on soil bacterial community structure. FEMS Microbiology Ecology, 2002, 42(3): 387–397

    Article  CAS  Google Scholar 

  45. Wu J F, Jiang C Y, Wang B J, Ma Y F, Liu Z P, Liu S J. Novel partial reductive pathway for 4-chloronitrobenzene and nitrobenzene degradation in Comamonas sp. strain CNB-1. Applied and Environmental Microbiology, 2006, 72(3): 1759–1765

    Article  CAS  Google Scholar 

  46. Ma Y F, Wu J F, Wang S Y, Jiang C Y, Zhang Y, Qi S W, Liu L, Zhao G P, Liu S J. Nucleotide sequence of plasmid pCNB1 from Comamonas strain CNB-1 reveals novel genetic organization and evolution for 4-chloronitrobenzene degradation. Applied and Environmental Microbiology, 2007, 73(14): 4477–4483

    Article  CAS  Google Scholar 

  47. Xiao Y, Liu T T, Dai H, Zhang J J, Liu H, Tang H, Leak D J, Zhou N Y. OnpA, an unusual flavin-dependent monooxygenase containing a cytochrome b5 domain. Journal of Bacteriology, 2012, 194(6): 1342–1349

    Article  CAS  Google Scholar 

  48. Kästner M, Breuer-Jammali M, Mahro B. Impact of inoculation protocols, salinity, and pH on the degradation of polycyclic aromatic hydrocarbons (PAHs) and survival of PAH-degrading bacteria introduced into soil. Applied and Environmental Microbiology, 1998, 64(1): 359–362

    Google Scholar 

  49. Choi H, Harrison R, Komulainen H, Delgado-Saborit J M. Polycyclic aromatic hydrocarbons. In: World Health Organization, Regional Office for Europe, eds. Selected Pollutants: WHO Guidelines for Indoor Air Quality. Geneva: World Health Organization, 2010, 289–325

    Google Scholar 

  50. Johnsen A R, Wick L Y, Harms H. Principles of microbial PAHdegradation in soil. Environmental Pollution, 2005, 133(1): 71–84

    Article  CAS  Google Scholar 

  51. Yu S H, Ke L, Wong Y S, Tam N F Y. Degradation of polycyclic aromatic hydrocarbons by a bacterial consortium enriched from mangrove sediments. Environment International, 2005, 31(2): 149–154

    Article  CAS  Google Scholar 

  52. Gramss G, Voigt K D, Kirsche B. Degradation of polycyclic aromatic hydrocarbons with three to seven aromatic rings by higher fungi in sterile and unsterile soils. Biodegradation, 1999, 10(1): 51–62

    Article  CAS  Google Scholar 

  53. Bamforth S M, Singleton I. Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. Journal of Chemical Technology and Biotechnology (Oxford, Oxfordshire), 2005, 80(7): 723–736

    Article  CAS  Google Scholar 

  54. Eibes G, Cajthaml T, Moreira M T, Feijoo G, Lema J M. Enzymatic degradation of anthracene, dibenzothiophene and pyrene by manganese peroxidase in media containing acetone. Chemosphere, 2006, 64(3): 408–414

    Article  CAS  Google Scholar 

  55. Silva I S, Grossman M, Durranta L R. Degradation of polycyclic aromatic hydrocarbons (2–7 rings) under microaerobic and verylow-oxygen conditions by soil fungi. International Biodeterioration & Biodegradation, 2009, 63(2): 224–229

    Article  CAS  Google Scholar 

  56. Garon D, Sage L, Wouessidjewe D, Seigle-Murandi F. Enhanced degradation of fluorene in soil slurry by Absidia cylindrospora and maltosyl-cyclodextrin. Chemosphere, 2004, 56(2): 159–166

    Article  CAS  Google Scholar 

  57. Potin O, Rafin C, Veignie E. Bioremediation of an aged polycyclic aromatic hydrocarbons (PAHs)-contaminated soil by flamentous fungi isolated from the soil. International Biodeterioration & Biodegradation, 2004, 54(1): 45–52

    Article  CAS  Google Scholar 

  58. Jacques R J S, Okeke B C, Bento FM, Teixeira A S, Peralba M C R, Camargo F A O. Microbial consortium bioaugmentation of a polycyclic aromatic hydrocarbons contaminated soil. Bioresource Technology, 2008, 99(7): 2637–2643

    Article  CAS  Google Scholar 

  59. Jacques R J S, Okeke B C, Bento FM, PeralbaMC R, Camargo F A O. Characterization of a polycyclic aromatic hydrocarbon degrading microbial consortium from a petrochemical sludge landfarming site. Bioremediation Journal, 2007, 11(1): 1–11

    Article  CAS  Google Scholar 

  60. Silva I S, Santos E C, Menezes C R, Faria A F, Franciscon E, Grossman M, Durrant L R. Bioremediation of a polyaromatic hydrocarbon contaminated soil by native soil microbiota and bioaugmentation with isolated microbial consortia. Bioresource Technology, 2009, 100(20): 4669–4675

    Article  CAS  Google Scholar 

  61. Pemberton J M, Corney B, Don R H. Evolution and spread of pesticide degrading ability among soil micro-organisms, In: Timmis KN, Puhler A, eds. Plasmids of Medical, Environmental and Commercial Importance. Amsterdam, Netherlands: Elsevier/North- Holland Biomedical, 1979, 287–299

    Google Scholar 

  62. Don R H, Pemberton J M. Genetic and physical map of the 2,4- dichlorophenoxyacetic acid-degradative plasmid pJP4. Journal of Bacteriology, 1985, 161(1): 466–468

    CAS  Google Scholar 

  63. Daane L L, Häggblom M M. Earthworm egg capsules as vectors for the environmental introduction of biodegradative bacteria. Applied and Environmental Microbiology, 1999, 65(6): 2376–2381

    CAS  Google Scholar 

  64. Nam K, Kukor J J. Combined ozonation and biodegradation for remediation of mixtures of polycyclic aromatic hydrocarbons in soil. Biodegradation, 2000, 11(1): 1–9

    Article  CAS  Google Scholar 

  65. Bouchez T, Patureau D, Dabert P, Juretschko S, Doré J, Delgenès P, Moletta R, Wagner M. Ecological study of a bioaugmentation failure. Environmental Microbiology, 2000, 2(2): 179–190

    Article  CAS  Google Scholar 

  66. Singer A C, van der Gast C J, Thompson I P. Perspectives and vision for strain selection in bioaugmentation. Trends in Biotechnology, 2005, 23(2): 74–77

    Article  CAS  Google Scholar 

  67. Cunliffe M, Kertesz M A. Effect of Sphingobium yanoikuyae B1 inoculation on bacterial community dynamics and polycyclic aromatic hydrocarbon degradation in aged and freshly PAHcontaminated soils. Environmental Pollution, 2006, 144(1): 228–237

    Article  CAS  Google Scholar 

  68. Chi X Q, Liu K, Zhou N Y. Effects of bioaugmentation in paranitrophenol- contaminated soil on the abundance and community structure of ammonia-oxidizing bacteria and archaea. Applied Microbiology and Biotechnology, 2015, 99(14): 6069–6082

    Article  CAS  Google Scholar 

  69. Kennedy T A, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P. Biodiversity as a barrier to ecological invasion. Nature, 2002, 417(6889): 636–638

    Article  CAS  Google Scholar 

  70. Mrozik A, Piotrowska-Seget Z. Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. Microbiological Research, 2010, 165(5): 363–375

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Microbial Metabolism & School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China

    Ying Xu & Ning-Yi Zhou

Authors
  1. Ying Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ning-Yi Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ning-Yi Zhou.

Additional information

Professor Ning-Yi Zhou received his Bachelor’s degree in Microbiology from Wuhan University and PhD in Microbiology from Imperial College London. Following postdoctoral training at Imperial College and University of Wales, Bangor, Prof. Zhou established his own laboratory in Wuhan Institute of Virology of Chinese Academy of Sciences. He has recently joined Shanghai Jiao Tong University as a distinguished professor. Over the last two decades, his research has been focusing on the genetics and biochemistry of microbial aromatic catabolism in various bacteria as well as the bioaugmentation of contaminated soil with microbial degraders, publishing more than 70 papers in this field. Currently, he serves an editor for “Applied and Environmental Microbiology” and an associate editor for “Frontiers in Microbiology”. He was among the most cited Chinese researchers listed by Elsevier for 2014 and 2015 (Microbiology & Immunology Section).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Y., Zhou, NY. Microbial remediation of aromatics-contaminated soil. Front. Environ. Sci. Eng. 11, 1 (2017). https://doi.org/10.1007/s11783-017-0894-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-017-0894-x

Keywords

Search

Navigation