Microbial remediation of aromatics-contaminated soil

Abstract

Aromatics-contaminated soils were successfully remediated with adding single strains.

Bacterial or fungal consortia were successfully used in the cases of bioaugmentation.

Microbes combined with chemical or biological factors increase remediation efficiency.

The environmental factors had appreciable impacts on the bioaugmentation.

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.

Graphical abstract

Keywords

Aromatics-contaminated soil / Bacteria / Bioaugmentation / Bioremediation / Fungi

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

[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

[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

[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

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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

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

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

[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

[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

[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

[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

[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

[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

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

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

[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

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

[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

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

[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

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

[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

[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

[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

[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

[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

[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

[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

[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

[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

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

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

[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

[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

[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

[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

[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

[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

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

[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

[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

[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

[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

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

[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

[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

[58] Jacques R J S, Okeke B C, Bento F M, 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

[59] Jacques R J S, Okeke B C, Bento F M, Peralba M C 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

[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

[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

[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

[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

[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

[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

[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

[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 PAH-contaminated soils. Environmental Pollution, 2006, 144(1): 228–237

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

[69] Kennedy T A, Naeem S, Howe K M, Knops J M H, Tilman D, Reich P. Biodiversity as a barrier to ecological invasion. Nature, 2002, 417(6889): 636–638

[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

Acknowledgements

This work is supported by the National Key Research and Development Program of China (No. 2016YFA0601102) and the National Natural Science Foundation of China (Grant Nos. 31370094 and 31570100).

Funding

RIGHTS & PERMISSIONS

2017 Higher Education Press and Springer-Verlag Berlin Heidelberg