Anaerobic phenanthrene biodegradation with four kinds of electron acceptors enriched from the same mixed inoculum and exploration of metabolic pathways

Zuotao Zhang , Chongyang Wang , Jianzhong He , Hui Wang

Front. Environ. Sci. Eng. ›› 2019, Vol. 13 ›› Issue (5) : 80

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Front. Environ. Sci. Eng. ›› 2019, Vol. 13 ›› Issue (5) : 80 DOI: 10.1007/s11783-019-1164-x
RESEARCH ARTICLE
RESEARCH ARTICLE

Anaerobic phenanthrene biodegradation with four kinds of electron acceptors enriched from the same mixed inoculum and exploration of metabolic pathways

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Abstract

Anaerobic phenanthrene biodegradation enriched process was described in detail.

The enriched bacterial communities were characterized under four redox conditions.

The enriched archaeal communities were stated under high percentage conditions.

Relatively intact pathways of anaerobic phenanthrene biodegradation were proposed.

Polycyclic aromatic hydrocarbons (PAHs) are widespread and persistent contaminants worldwide, especially in environments devoid of molecular oxygen. For lack of molecular oxygen, researchers enhanced anaerobic zones PAHs biodegradation by adding sulfate, bicarbonate, nitrate, and iron. However, microbial community reports of them were limited, and information of metabolites was poor except two-ring PAH, naphthalene. Here, we reported on four phenanthrene-degrading enrichment cultures with sulfate, bicarbonate, nitrate, and iron as electron acceptors from the same initial inoculum. The high-to-low order of the anaerobic phenanthrene biodegradation rate was the nitrate-reducing conditions>sulfate-reducing conditions>methanogenic conditions>iron-reducing conditions. The dominant bacteria populations were Desulfobacteraceae, Anaerolinaceae, and Thermodesulfobiaceae under sulfate-reducing conditions; Moraxellaceae, Clostridiaceae, and Comamonadaceae under methanogenic conditions; Rhodobacteraceae, Planococcaceae, and Xanthomonadaceae under nitrate-reducing conditions; and Geobacteraceae, Carnobacteriaceae, and Anaerolinaceae under iron-reducing conditions, respectively. Principal component analysis (PCA) indicated that bacteria populations of longtime enriched cultures with four electron acceptors all obtained significant changes from original inoculum, and bacterial communities were similar under nitrate-reducing and iron-reducing conditions. Archaea accounted for a high percentage under iron-reducing and methanogenic conditions, and Methanosarcinaceae and Methanobacteriaceae, as well as Methanobacteriaceae, were the dominant archaea populations under iron-reducing and methanogenic conditions. The key steps of phenanthrene biodegradation under four reducing conditions were carboxylation, further ring system reduction, and ring cleavage.

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Keywords

Phenanthrene / Anaerobic biodegradation / Bacterial populations / Archaea populations / Metabolic pathway

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Zuotao Zhang, Chongyang Wang, Jianzhong He, Hui Wang. Anaerobic phenanthrene biodegradation with four kinds of electron acceptors enriched from the same mixed inoculum and exploration of metabolic pathways. Front. Environ. Sci. Eng., 2019, 13(5): 80 DOI:10.1007/s11783-019-1164-x

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References

[1]

Amann R, Fuchs B M (2008). Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nature Reviews. Microbiology, 6(5): 339–348

[2]

Annweiler E, Michaelis W, Meckenstock R U (2002). Identical ring cleavage products during anaerobic degradation of naphthalene, 2-methylnaphthalene, and tetralin indicate a new metabolic pathway. Applied and Environmental Microbiology, 68(2): 852–858

[3]

APHA (1998). Standard Methods for the Examination of Water and Wastewater. Baltimore MD: American Public Health Association

[4]

Bauer J E, Capone D G (1985). Degradation and mineralization of the polycyclic aromatic hydrocarbons anthracene and naphthalene in intertidal marine sediments. Applied and Environmental Microbiology, 50(1): 81–90

[5]

Berdugo-Clavijo C, Dong X, Soh J, Sensen C W, Gieg L M (2012). Methanogenic biodegradation of two-ringed polycyclic aromatic hydrocarbons. FEMS Microbiology Ecology, 81(1): 124–133

[6]

Chang B V, Chang S W, Yuan S Y (2003). Anaerobic degradation of polycyclic aromatic hydrocarbons in sludge. Advances in Environmental Research, 7(3): 623–628

[7]

Coates J D, Anderson R T, Woodward J C, Phillips E J P, Lovley D R (1996). Anaerobic hydrocarbon degradation in petroleum-contaminated harbor sediments under sulfate-reducing and artificially imposed iron-reducing conditions. Environmental Science & Technology, 30(9): 2784–2789

[8]

Davidova I A, Gieg L M, Duncan K E, Suflita J M (2007). Anaerobic phenanthrene mineralization by a carboxylating sulfate-reducing bacterial enrichment. The ISME journal, 1(5): 436–442

[9]

Fang T, Pan R, Jiang J, He F, Wang H (2016). Effect of salinity on community structure and naphthalene dioxygenase gene diversity of a halophilic bacterial consortium. Frontiers of Environmental Science & Engineering, 10(6): 16

[10]

Feng Z J, Zhu L Z (2018). Sorption of phenanthrene to biochar modified by base. Frontiers of Environmental Science & Engineering, 12 (2): 1 doi:10.1007/s11783-017-0978-7

[11]

Fuchedzhieva N, Karakashev D, Angelidaki I (2008). Anaerobic biodegradation of fluoranthene under methanogenic conditions in presence of surface-active compounds. Journal of Hazardous Materials, 153(1–2): 123–127

[12]

Galushko A, Minz D, Schink B, Widdel F (1999). Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulphate-reducing bacterium. Environmental Microbiology, 1(5): 415–420

[13]

Hambrick G A, Delaune R D, Patrick W H (1980). Effect of estuarine sediment pH and oxidation-reduction potential on microbial hydrocarbon degradation. Applied and Environmental Microbiology, 40(2): 365–369

[14]

Himmelberg A M, Brüls T, Farmani Z, Weyrauch P, Barthel G, Schrader W, Meckenstock R U (2018). Anaerobic degradation of phenanthrene by a sulfate-reducing enrichment culture. Environmental Microbiology, 20(10): 3589–3600

[15]

Kleemann R, Meckenstock R U (2011). Anaerobic naphthalene degradation by Gram-positive, iron-reducing bacteria. FEMS Microbiology Ecology, 78(3): 488–496

[16]

Kümmel S, Herbst F A, Bahr A, Duarte M, Pieper D H, Jehmlich N, Seifert J, von Bergen M, Bombach P, Richnow H H, Vogt C (2015). Anaerobic naphthalene degradation by sulfate-reducing Desulfobacteraceae from various anoxic aquifers. FEMS Microbiology Ecology, 91(3): 1 12: fiv006

[17]

Langenhoff A A M, Zehnder A J B, Schraa G (1996). Behaviour of toluene, benzene and naphthalene under anaerobic conditions in sediment columns. Biodegradation, 7(3): 267–274

[18]

Li J, Luo C, Song M, Dai Q, Jiang L, Zhang D, Zhang G (2017). Biodegradation of phenanthrene in polycyclic aromatic hydrocarbon-contaminated wastewater revealed by coupling cultivation-dependent and-independent approaches. Environmental Science & Technology, 51(6): 3391–3401

[19]

Luo F, Gitiafroz R, Devine C E, Gong Y, Hug L A, Raskin L, Edwards E A (2014). Metatranscriptome of an anaerobic benzene-degrading, nitrate-reducing enrichment culture reveals involvement of carboxylation in benzene ring activation. Applied and Environmental Microbiology, 80(14): 4095–4107

[20]

Luo J, Zhang J, Tan X, McDougald D, Zhuang G, Fane A G, Kjelleberg S, Cohen Y, Rice S A (2015). Characterization of the archaeal community fouling a membrane bioreactor. Journal of Environmental Sciences-China, 29: 115–123

[21]

Martirani-Von Abercron S M, Pacheco D, Benito-Santano P, Marín P, Marqués S (2016). Polycyclic aromatic hydrocarbon-induced changes in bacterial community structure under anoxic nitrate reducing conditions. Frontiers in Microbiology, 7: 1–16

[22]

Meckenstock R U, Annweiler E, Michaelis W, Richnow H H, Schink B (2000). Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Applied and Environmental Microbiology, 66(7): 2743–2747

[23]

Mihelcic J R, Luthy R G (1988). Degradation of polycyclic aromatic hydrocarbon compounds under various redox conditions in soil-water systems. Applied and Environmental Microbiology, 54(5): 1182–1187

[24]

Morris B E, Gissibl A, Kümmel S, Richnow H H, Boll M (2014). A PCR-based assay for the detection of anaerobic naphthalene degradation. FEMS Microbiology Letters, 354(1): 55–59

[25]

Mouttaki H, Johannes J, Meckenstock R U (2012). Identification of naphthalene carboxylase as a prototype for the anaerobic activation of non-substituted aromatic hydrocarbons. Environmental Microbiology, 14(10): 2770–2774

[26]

Müller J B, Ramos D T, Larose C, Fernandes M, Lazzarin H S, Vogel T M, Corseuil H X (2017). Combined iron and sulfate reduction biostimulation as a novel approach to enhance BTEX and PAH source-zone biodegradation in biodiesel blend-contaminated groundwater. Journal of Hazardous Materials, 326: 229–236

[27]

Musat F, Galushko A, Jacob J, Widdel F, Kube M, Reinhardt R, Wilkes H, Schink B, Rabus R (2009). Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria. Environmental Microbiology, 11(1): 209–219

[28]

Obi C C, Adebusoye S A, Amund O O, Ugoji E O, Ilori M O, Hedman C J, Hickey W J (2017). Structural dynamics of microbial communities in polycyclic aromatic hydrocarbon-contaminated tropical estuarine sediments undergoing simulated aerobic biotreatment. Applied Microbiology and Biotechnology, 101(10): 4299–4314

[29]

Rockne K J, Strand S E (2001). Anaerobic biodegradation of naphthalene, phenanthrene, and biphenyl by a denitrifying enrichment culture. Water Research, 35(1): 291–299

[30]

Safinowski M, Meckenstock R U (2006). Methylation is the initial reaction in anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Environmental Microbiology, 8(2): 347–352

[31]

Sharak Genthner B R, Townsend G T, Lantz S E, Mueller J G (1997). Persistence of polycyclic aromatic hydrocarbon components of creosote under anaerobic enrichment conditions. Archives of Environmental Contamination and Toxicology, 32(1): 99–105

[32]

Smith M R (1990). The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation, 1(2–3): 191–206

[33]

Tor J M, Lovley D R (2001). Anaerobic degradation of aromatic compounds coupled to Fe(III) reduction by Ferroglobus placidus. Environmental Microbiology, 3(4): 281–287

[34]

Trably E, Patureau D, Delgenes J P (2003). Enhancement of polycyclic aromatic hydrocarbons removal during anaerobic treatment of urban sludge. Water Science and Technology, 48(4): 53–60

[35]

Weyrauch P, Zaytsev A V, Stephan S, Kocks L, Schmitz O J, Golding B T, Meckenstock R U (2017). Conversion of cis-2-carboxycyclohexylacetyl-CoA in the downstream pathway of anaerobic naphthalene degradation. Environmental Microbiology, 19(7): 2819–2830

[36]

Xu M, He Z, Zhang Q, Liu J, Guo J, Sun G, Zhou J (2015). Responses of aromatic-degrading microbial communities to elevated nitrate in sediments. Environmental Science & Technology, 49(20): 12422–12431

[37]

Yarza P, Yilmaz P, Pruesse E, Glöckner F O, Ludwig W, Schleifer K H, Whitman W B, Euzéby J, Amann R, Rosselló-Móra R (2014). Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nature Reviews. Microbiology, 12(9): 635–645

[38]

Ye Q H, Wang C Y, Wang Y, Wang H (2018). Characterization of a phenanthrene-degrading methanogenic community. Frontiers of Environmental Science & Engineering, 12 (5): 4 doi: 10.1007/s11783-018-1083-2

[39]

Yuan S Y, Chang B V (2007). Anaerobic degradation of five polycyclic aromatic hydrocarbons from river sediment in Taiwan. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 42(1): 63–69

[40]

Zhang S Y, Wang Q F, Xie S G (2012). Molecular characterization of phenanthrene-degrading methanogenic communities in leachate-contaminated aquifer sediment. International Journal of Environmental Science and Technology, 9(4): 705–712

[41]

Zhang X, Sullivan E R, Young L Y (2000). Evidence for aromatic ring reduction in the biodegradation pathway of carboxylated naphthalene by a sulfate reducing consortium. Biodegradation, 11(2/3): 117–124

[42]

Zhang X, Young L Y (1997). Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Applied and Environmental Microbiology, 63(12): 4759–4764

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