Please wait a minute...
Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2018, Vol. 12 Issue (5) : 4    https://doi.org/10.1007/s11783-018-1083-2
RESEARCH ARTICLE
Characterization of a phenanthrene-degrading methanogenic community
Quanhui Ye, Chengyue Liang, Chongyang Wang, Yun Wang, Hui Wang()
State Key Joint Laboratory on Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China*
 Download: PDF(811 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

The mixed samples of contaminated soil, sludge and coke wastewater showed great phenanthrene methanogenic degradation potential.

Comamonadaceae, Nocardiaceae and Methanobacterium were dominant members.

Hexane, hexadecane and benzene could enhance phenanthrene degradation.

Polycyclic aromatic hydrocarbons (PAHs) often occur in oil-contaminated soil, coke wastewater and domestic sludge; however, associated PAH degraders in these environments are not clear. Here we evaluated phenanthrene degradation potential in the mixed samples of above environments, and obtained a methanogenic community with different microbial profile compared to those from sediments. Phenanthrene was efficiently degraded (1.26 mg/L/d) and nonstoichiometric amount of methane was produced simultaneously. 16S rRNA gene sequencing demonstrated that bacterial populations were mainly associated with Comamonadaceae Nocardiaceae and Thermodesulfobiaceae, and that methanogenic archaea groups were dominated by Methanobacterium and Methanothermobacter. Substances such as hexane, hexadecane, benzene and glucose showed the most positive effects on phenanthrene degradation. Substrate utilization tests indicated that this culture could not utilize other PAHs. These analyses could offer us some suggestions on the putative phenanthrene-degrading microbes in such environments, and might help us develop strategies for the removal of PAHs from contaminated soil and sludge.

Keywords Phenanthrene degradation potential      Methanogenic      Bacterial population      Archaeal group     
Corresponding Author(s): Hui Wang   
Issue Date: 21 September 2018
 Cite this article:   
Quanhui Ye,Chengyue Liang,Chongyang Wang, et al. Characterization of a phenanthrene-degrading methanogenic community[J]. Front. Environ. Sci. Eng., 2018, 12(5): 4.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-018-1083-2
https://academic.hep.com.cn/fese/EN/Y2018/V12/I5/4
Fig.1  Phenanthrene degradation rates of zero-order reaction in big flask during different enrichment phases; (phase 1: day 0–5; phase 2: day 7–13; phase 3: day 15?24; phase 4: day 25?39; phase 5: day 45?61; phase 6: day 66?80; phase 7: day 81?101; phase 8: day 105?121; phase 9: day 126?136; phase 10: day 137?155; phase 11: day 158?176; phase 12: day 180?198).
Fig.2  Bacterial members of the initial sample and of the methanogenic enrichment culture; (A) Bacterial groups at class level; (B) Bacterial groups at family level.
Fig.3  Archaeal members at genus level of the initial sample and of the methanogenic enrichment culture; (A) Archaeal groups of initial mixed samples; (B) Archaeal groups of methanogenic enrichment culture.
Fig.4  Relationship of phenanthrene degradation and methane production.
Substrate degradation capability
Benzene +
Naphthalene -
2-methylnaphthalene -
Phenanthrenecarboxylic acid +
Phenanthrene +
Anthracene ?
Fluoranthene ?
Pyrene ?
Tab.1  Substrate utilization tests
Treatment K K change
Inoculated control 0.031
Hexane 0.053 67.87%
Hexadecane 0.062 96.60%
Benzene 0.052 65.39%
Phenanthrenecarboxylic acid 0.045 44.62%
Sodium propionate 0.042 34.92%
Sodium acetate 0.031 0.12%
Glucose 0.053 69.29%
Fulvic acid 0.031 ?0.23%
Humic acid 0.039 24.18%
AQDS 0.045 42.57%
BES 0.021 ?31.53%
Magnetite 0.039 23.22%
SDS 0.049 55.98%
L-rhamnose 0.048 54.34%
Twain-80 0.017 -47.42%
Tab.2  Effects of different substances on phenanthrene degradation rate (K)
1 Aislabie J, McLeod M, Fraser R (1998). Potential for biodegradation of hydrocarbons in soil from the Ross Dependency, Antarctica. Applied Microbiology and Biotechnology, 49(2): 210–214
https://doi.org/10.1007/s002530051160
2 Bengtsson G, Zerhouni P (2003). Effects of carbon substrate enrichment and DOC concentration on biodegradation of PAHs in soil. Journal of Applied Microbiology, 94(4): 608–617
https://doi.org/10.1046/j.1365-2672.2003.01873.x pmid: 12631196
3 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
https://doi.org/10.1111/j.1574-6941.2012.01328.x pmid: 22324881
4 Canul-Chan M, Sánchez-González M, González-Burgos A, Zepeda A, Rojas-Herrera R (2017). Population structures shift during the biodegradation of crude and fuel oil by an indigenous consortium. International Journal of Environmental Science and Technology, 15(1): 1–16
https://doi.org/10.1007/s13762-017-1362-7
5 Chang B V, Chang I T, Yuan S Y (2008a). Anaerobic degradation of phenanthrene and pyrene in mangrove sediment. Bulletin of Environmental Contamination and Toxicology, 80(2): 145–149
https://doi.org/10.1007/s00128-007-9333-1 pmid: 18188486
45 Chang B V, Chang S W, Yuan S Y. Anaerobic degradation of polycyclic aromatic hydrocarbons in sludge. Adv Environ Res, 2003, 7(3): 623–628
46 Chang B V, Shiung L C, Yuan S Y. Anaerobic biodegradation of polycyclic aromatic hydrocarbon in soil. Chemosphere, 2002, 48: 717–724
6 Chang M W, Holoman T P, Yi H (2008b). Molecular characterization of surfactant-driven microbial community changes in anaerobic phenanthrene-degrading cultures under methanogenic conditions. Biotechnology Letters, 30(9): 1595–1601
https://doi.org/10.1007/s10529-008-9731-4 pmid: 18421419
7 Chang W, Um Y, Hoffman B, Pulliam Holoman T R (2005). Molecular characterization of polycyclic aromatic hydrocarbon (PAH)-degrading methanogenic communities. Biotechnology Progress, 21(3): 682–688
https://doi.org/10.1021/bp049579l pmid: 15932243
8 Chang W, Um Y, Holoman T R (2006). Polycyclic aromatic hydrocarbon (PAH) degradation coupled to methanogenesis. Biotechnology Letters, 28(6): 425–430
https://doi.org/10.1007/s10529-005-6073-3 pmid: 16614909
9 Chen S, Aitken M D (1999). Salicylate stimulates the degradation of high-molecular weight polycyclic aromatic hydrocarbons by Pseudomonas saccharophila P15. Environmental Science & Technology, 33(3): 435–439
https://doi.org/10.1021/es9805730
10 Davidova I A, Gieg L M, Duncan K E, Suflita J M (2007). Anaerobic phenanthrene mineralization by a carboxylating sulfate-reducing bacterial enrichment. ISME Journal, 1(5): 436–442
https://doi.org/10.1038/ismej.2007.48 pmid: 18043662
11 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
https://doi.org/10.1007/s11783-016-0888-0
12 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
https://doi.org/10.1016/j.jhazmat.2007.08.027 pmid: 17869417
13 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
https://doi.org/10.1046/j.1462-2920.1999.00051.x pmid: 11207761
14 Gómez R S G, Pandiyan T, Iris V E A, Luna-Pabello V, de Bazúa C D (2004). Spectroscopic determination of poly-aromatic compounds in petroleum contaminated soils. Water, Air, and Soil Pollution, 158(1): 137–151
https://doi.org/10.1023/B:WATE.0000044829.26130.1c
15 Goyal A K, Zylstra G J (1996). Molecular cloning of novel genes for polycyclic aromatic hydrocarbon degradation from Comamonas testosteroni GZ39. Applied and Environmental Microbiology, 62(1): 230–236
pmid: 8572701
16 Gray N D, Sherry A, Larter S R, Erdmann M, Leyris J, Liengen T, Beeder J, Head I M (2009). Biogenic methane production in formation waters from a large gas field in the North Sea. Extremophiles, 13(3): 511–519
https://doi.org/10.1007/s00792-009-0237-3 pmid: 19305943
17 Haritash A K, Kaushik C P (2009). Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. Journal of Hazardous Materials, 169(1-3): 1–15
https://doi.org/10.1016/j.jhazmat.2009.03.137 pmid: 19442441
18 Huang Y, Zhang J, Zhu L (2013). Evaluation of the application potential of bentonites in phenanthrene bioremediation by characterizing the biofilm community. Bioresource Technology, 134: 17–23
https://doi.org/10.1016/j.biortech.2013.02.009 pmid: 23500554
19 Jiménez N, Viñas M, Bayona J M, Albaiges J, Solanas A M (2007). The Prestige oil spill: bacterial community dynamics during a field biostimulation assay. Applied Microbiology and Biotechnology, 77(4): 935–945
https://doi.org/10.1007/s00253-007-1229-9 pmid: 17943279
20 Keith L H, Telliard W A (1979). Priority pollutants I—A perspective view. Environmental Science & Technology, 13(4): 416–423
https://doi.org/10.1021/es60152a601
21 Kong X, Yu S, Xu S, Fang W, Liu J, Li H (2018). Effect of Fe0 addition on volatile fatty acids evolution on anaerobic digestion at high organic loading rates. Waste Management (New York, N.Y.), 71: 719–727
https://doi.org/10.1016/j.wasman.2017.03.019 pmid: 28320620
22 Kryachko Y, Dong X, Sensen C W, Voordouw G (2012). Compositions of microbial communities associated with oil and water in a mesothermic oil field. Antonie van Leeuwenhoek, 101(3): 493–506
https://doi.org/10.1007/s10482-011-9658-y pmid: 22038128
23 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): 1–13
https://doi.org/10.1093/femsec/fiv006 pmid: 25764566
24 Li H, Chang J, Liu P, Fu L, Ding D, Lu Y (2015). Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments. Environmental Microbiology, 17(5): 1533–1547
https://doi.org/10.1111/1462-2920.12576 pmid: 25059331
25 Liang B, Wang L Y, Mbadinga S M, Liu J F, Yang S Z, Gu J D, Mu B Z (2015). Anaerolineaceae and Methanosaeta turned to be the dominant microorganisms in alkanes-dependent methanogenic culture after long-term of incubation. AMB Express, 5(1): 117
https://doi.org/10.1186/s13568-015-0117-4 pmid: 26080793
26 Lladó S, Jiménez N, Viñas M, Solanas A M (2009). Microbial populations related to PAH biodegradation in an aged biostimulated creosote-contaminated soil. Biodegradation, 20(5): 593–601
https://doi.org/10.1007/s10532-009-9247-1 pmid: 19153811
27 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
https://doi.org/10.1016/j.jes.2014.07.025 pmid: 25766019
28 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
https://doi.org/10.1111/j.1462-2920.2008.01756.x pmid: 18811643
29 Pérez S, Guillamón M, Barceló D (2001). Quantitative analysis of polycyclic aromatic hydrocarbons in sewage sludge from wastewater treatment plants. Journal of Chromatography. A, 938(1-2): 57–65
https://doi.org/10.1016/S0021-9673(01)01338-3 pmid: 11771847
30 Pinyakong O, Tiangda K, Iwata K, Omori T (2012). Isolation of novel phenanthrene-degrading bacteria from seawater and the influence of its physical factors on the degradation of phenanthrene. Science Asia, 38(1): 36–43
https://doi.org/10.2306/scienceasia1513-1874.2012.38.036
31 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
https://doi.org/10.1111/j.1462-2920.2005.00900.x pmid: 16423020
32 Sekiguchi Y, Kamagata Y, Syutsubo K, Ohashi A, Harada H, Nakamura K (1998). Phylogenetic diversity of mesophilic and thermophilic granular sludges determined by 16S rRNA gene analysis. Microbiology-Uk, 144(Pt 9): 2655–2665
https://doi.org/10.1099/00221287-144-9-2655 pmid: 9782515
33 Sullivan E R, Zhang X, Phelps C, Young L Y (2001). Anaerobic mineralization of stable-isotope-labeled 2-methylnaphthalene. Applied and Environmental Microbiology, 67(9): 4353–4357
https://doi.org/10.1128/AEM.67.9.4353-4357.2001 pmid: 11526046
34 Tøndervik A, Bruheim P, Berg L, Ellingsen T E, Kotlar H K, Valla S, Throne-Holst M (2012). Ralstonia sp. U2 naphthalene dioxygenase and Comamonas sp. JS765 nitrobenzene dioxygenase show differences in activity towards methylated naphthalenes. Journal of Bioscience and Bioengineering, 113(2): 173–178
https://doi.org/10.1016/j.jbiosc.2011.10.001 pmid: 22036075
35 Wan R, Zhang S, Xie S (2012). Microbial community changes in aquifer sediment microcosm for anaerobic anthracene biodegradation under methanogenic condition. Journal of Environmental Sciences (China), 24(8): 1498–1503
https://doi.org/10.1016/S1001-0742(11)60959-5 pmid: 23513693
36 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
https://doi.org/10.1038/nrmicro3330 pmid: 25118885
37 Ye Q, Zhang Z, Huang Y, Fang T, Cui Q, He C, Wang H (2018). Enhancing electron transfer by magnetite during phenanthrene anaerobic methanogenic degradation. International Biodeterioration & Biodegradation, 129: 109–116
https://doi.org/10.1016/j.ibiod.2018.01.012
38 Yin Q, Miao J, Li B, Wu G (2017). Enhancing electron transfer by ferroferric oxide during the anaerobic treatment of synthetic wastewater with mixed organic carbon. International Biodeterioration & Biodegradation, 119: 104–110
https://doi.org/10.1016/j.ibiod.2016.09.023
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
https://doi.org/10.1080/03601230601020860 pmid: 17162569
40 Zhang S, Wang Q, Xie S (2012a). Stable isotope probing identifies anthracene degraders under methanogenic conditions. Biodegradation, 23(2): 221–230
https://doi.org/10.1007/s10532-011-9501-1 pmid: 21805116
41 Zhang S Y, Wang Q F, Xie S G (2012b). Molecular characterization of phenanthrene-degrading methanogenic communities in leachate-contaminated aquifer sediment. International Journal of Environmental Science and Technology, 9(4): 705–712
https://doi.org/10.1007/s13762-012-0098-7
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
pmid: 9471963
43 Zhou S, Xu J, Yang G, Zhuang L (2014). Methanogenesis affected by the co-occurrence of iron(III) oxides and humic substances. FEMS Microbiology Ecology, 88(1): 107–120
https://doi.org/10.1111/1574-6941.12274 pmid: 24372096
44 Zhuang L, Tang J, Wang Y, Hu M, Zhou S (2015). Conductive iron oxide minerals accelerate syntrophic cooperation in methanogenic benzoate degradation. Journal of Hazardous Materials, 293: 37–45
https://doi.org/10.1016/j.jhazmat.2015.03.039 pmid: 25827267
[1] Supplementary Material 1 Download
[1] 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[J]. Front. Environ. Sci. Eng., 2019, 13(5): 80-.
[2] Guangqing Song, Hongbo Xi, Xiumei Sun, Yudong Song, Yuexi Zhou. Effect of 2-butenal manufacture wastewater to methanogenic activity and microbial community[J]. Front. Environ. Sci. Eng., 2018, 12(5): 10-.
[3] ZHOU Xuefei, REN Nanqi. Acid resistance of methanogenic bacteria in a two-stage anaerobic process treating high concentration methanol wastewater[J]. Front.Environ.Sci.Eng., 2007, 1(1): 53-56.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed