Association of growth substrates and bacterial genera with benzo[a]pyrene mineralization in contaminated soil

Environmental Engineering Science

Volumn 31, Issue 12, 2014, Pages 689-697

  Jones, Maiysha D ^a   Rodgers Vieira, Elyse A ^c   Hu, Jing ^b   Aitken, Michael D ^c  

^a PROCTER AND GAMBLE COMPANY   (United States)

^b DOW CHEMICAL COMPANY   (United States)

^c University of North Carolina at Chapel Hill   (United States)

Author keywords

Benzo a pyrene; bioremediation; cometabolism; PAHs; pyrosequencing; soil

Indexed keywords

ANTHRACENE; BACTERIA; BIOCONVERSION; BIOREACTORS; BIOREMEDIATION; MINERALOGY; NAPHTHALENE; POLYCYCLIC AROMATIC HYDROCARBONS; PYRENE; RNA; SOIL POLLUTION; SOILS; SUBSTRATES;

BACTERIAL COMMUNITY; BENZO [A] PYRENE; BENZ[A]ANTHRACENE; CO METABOLISMS; CONTAMINATED SOILS; POLYCYCLIC AROMATIC HYDROCARBON (PAH); PYROSEQUENCING; RELATIVE ABUNDANCE;

BARIUM COMPOUNDS;

ANTHRACENE; BENZO[A]PYRENE; BENZ[A]ANTHRACENE; FLUORANTHENE; NAPHTHALENE; PHENANTHRENE; PYRENE; RNA 16S;

ARTICLE; BACTERIAL GROWTH; BACTERIUM IDENTIFICATION; BIOREACTOR; BIOREMEDIATION; CUPRIAVIDUS; INCUBATION TIME; MICROBIAL COMMUNITY; MINERALIZATION; PYROSEQUENCING; SOIL POLLUTION;

BACTERIA (MICROORGANISMS);

EID: 84916213816     PISSN: 10928758     EISSN: 15579018     Source Type: Journal    
DOI: 10.1089/ees.2014.0275     Document Type: Article

References (53)

1. Aitken, M.D., Stringfellow, W.T., Nagel, R.D., Kazunga, C., and Chen, S.H. (1998). Characteristics of phenanthrenedegrading bacteria isolated from soils contaminated with polycyclic aromatic hydrocarbons. Can. J. Microbiol. 44, 743.
2. Beyea, J., Stellman, S.D., Hatch, M., and Gammon, M.D. (2008). Airborne emissions from 1961 to 2004 of benzo[a]-pyrene from U.S. vehicles per km of travel based on tunnel studies. Environ. Sci. Technol. 42, 7315.
3. Boonchan, S., Britz, M.L., and Stanley, G.A. (2000). Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by defined fungal-bacterial cocultures. Appl. Environ. Microbiol. 66, 1007.
4. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T.L. (2009). BLAST plus: architecture and applications. BMC Bioinformatics 10, 421.
5. Chen, S.H., and Aitken, M.D. (1999). Salicylate stimulates the degradation of high-molecular weight polycyclic aromatic hydrocarbons by Pseudomonas saccharophila P15. Environ. Sci. Technol. 33, 435.
6. Dries, J., and Smets, B.F. (2002). Transformation and mineralization of benzo[a]pyrene by microbial cultures enriched on mixtures of three-and four-ring polycyclic aromatic hydrocarbons. J. Ind. Microbiol. Biotechnol. 28, 70.
7. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011). Uchime improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194.
8. Finkmann, W., Altendorf, K., Stackebrandt, E., and Lipski, A. (2000). Characterization of N2O-producing Xanthomonaslike isolates from biofilters as Stenotrophomonas nitritireducens sp. nov., Luteimonas mephitis gen. nov., sp. nov. and Pseudoxanthomonas broegbernensis gen. nov., sp. nov. Int. J. Syst. Evol. Microbiol. 50, 273.
9. Hamady, M.,Walker, J.J., Harris, J.K., Gold, N.J., and Knight, R. (2008). Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat. Methods. 5, 235.
10. Han, B., Chen, Y., Abell, G., Jiang, H., Bodrossy, L., Zhao, J., Murrell, J.C., and Xing, X.-H. (2009). Diversity and activity of methanotrophs in alkaline soil from a Chinese coal mine. FEMS Microbiol. Ecol. 70, 196.
11. Hattemer-Frey, H.A., and Travis, C.C. (1991). Benzo-a-pyrene: environmental partitioning and human exposure. Toxicol. Ind. Health. 7, 141.
12. Hu, J., Nakamura, J., Richardson, S.D., and Aitken, M.D. (2012). Evaluating the effects of bioremediation on genotoxicity of polycyclic aromatic hydrocarbon-contaminated soil using genetically engineered, higher eukaryotic cell lines. Environ. Sci. Technol. 46, 4607.
13. IARC Working Group. (2010). IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Volume 92: Some Non-Heterocyclic Polycyclic Aromatic Hydrocarbons and Some Related Exposures. Lyon, France: World Health Organization, International Agency for Research on Cancer.
14. Jeon, C.O., Park, W., Ghiorse, W.C., and Madsen, E.L. (2004). Polaromonas naphthalenivorans sp. nov., a naphthalenedegrading bacterium from naphthalene-contaminated sediment. Int. J. Syst. Evol. Microbiol. 54, 93.
15. Jones, M.D., Crandell, D.W., Singleton, D.R., and Aitken, M.D. (2011a). Stable-isotope probing of the polycyclic aromatic hydrocarbon-degrading bacterial guild in a contaminated soil. Environ. Microbiol. 13, 2623.
16. Jones, M., Singleton, D., Carstensen, D., Powell, S., Swanson, J., Pfaender, F., and Aitken, M. (2008). Effect of incubation conditions on the enrichment of pyrene-degrading bacteria identified by stable-isotope probing in an aged, PAHcontaminated soil. Microb. Ecol. 56, 341.
17. Jones, M.D., Singleton, D.R., Sun, W., and Aitken, M.D. (2011b). Multiple DNA extractions coupled with stableisotope probing of anthracene-degrading bacteria in contaminated soil. Appl. Environ. Microbiol. 77, 2984.
18. Juhasz, A.L., Britz, M.L., and Stanley, G.A. (1997). Degradation of benzo[a]pyrene, dibenz[a,h]anthracene and coronene by Burkholderia cepacia. Water Sci. Technol. 34, 45.
19. Jurelevicius, D., Korenblum, E., Casella, R., Vital, R.L., and Seldin, L. (2010). Polyphasic analysis of the bacterial community in the rhizosphere and roots of Cyperus rotundus L. grown in a petroleum-contaminated soil. J. Microbiol. Biotechnol. 20, 862.
20. Kanaly, R.A., and Bartha, R. (1999). Cometabolic mineralization of benzo[a]pyrene caused by hydrocarbon additions to soil. Environ. Toxicol. Chem. 18, 2186.
21. Kasai, Y., Takahata, Y., Manefield, M., and Watanabe, K. (2006). RNA-based stable isotope probing and isolation of anaerobic benzene-degrading bacteria from gasolinecontaminated groundwater. Appl. Environ.Microbiol. 72, 3586.
22. Lane, D.J. (1991). 16S/23S rRNA Sequencing. In E. Stackebrandt and M. Goodfellow, Eds., Nucleic Acid Sequencing Techniques in Bacterial Systematics. New York, NY: John Wiley & Sons, pp. 115-175.
23. Lozupone, C., Hamady, M., and Knight, R. (2006). UniFrac: an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7, 371.
24. Luthy, R.G., Dzombak, D.A., Peters, C.A., Roy, S.B., Ramaswami, A., Nakles, D.V., and Nott, B.R. (1994). Remediating tar-contaminated soils at manufactured gas plant sites. Environ. Sci. Technol. 28, 266A.
25. Marcoux, J., Déziel, E., Villemur, R., Lépine, F., Bisaillon, J.G., and Beaudet, R. (2000). Optimization of high-molecularweight polycyclic aromatic hydrocarbons'degradation in a two-liquid-phase bioreactor. J. Appl. Microbiol. 88, 655.
26. Moody, J.D., Freeman, J.P., Fu, P.P., and Cerniglia, C.E. (2004). Degradation of benzo[a]pyrene by Mycobacterium vanbaalenii PYR-1. Appl. Environ. Microbiol. 70, 340.
27. Pérez-Pantoja, D., De la Iglesia, R., Pieper, D.H., and González, B. (2008). Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutantdegrading bacterium Cupriavidus necator JMP134. FEMS Microbiol. Rev. 32, 736.
28. Ping, L., Zhang, C., Zhang, C., Zhu, Y., He, H., Wu, M., Tang, T., Li, Z., and Zhao, H. (2014). Isolation and characterization of pyrene and benzo[a]pyrene-degrading Klebsiella pneumoniae PL1 and its potential use in bioremediation. Appl. Microbiol. Biotechnol. 98, 3819.
29. Popp, N., Schlomann,M., andMau,M. (2006). Bacterial diversity in the active stage of a bioremediation system for mineral oil hydrocarbon-contaminated soils. Microbiology 152, 3291.
30. Powell, S.N., Singleton, D.R., and Aitken, M.D. (2008). Effects of enrichment with salicylate on bacterial selection and PAH mineralization in a microbial community from a bioreactor treating contaminated soil. Environ. Sci. Technol. 42, 4099.
31. Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W.G., Peplies, J., and Glockner, F.O. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188.
32. Radajewski, S., Ineson, P., Parekh, N.R., and Murrell, J.C. (2000). Stable-isotope probing as a tool in microbial ecology. Nature 403, 646.
33. Rentz, J.A., Alvarez, P.J.J., and Schnoor, J.L. (2008). Benzo[a]-pyrene degradation by Sphingomonas yanoikuyae JAR02. Environ. Pollut. 151, 669.
34. Richardson, S.D., and Aitken, M.D. (2011). Desorption and bioavailability of PAHs in contaminated soil subjected to long-term in situ biostimulation. Environ. Toxicol. Chem. 30, 2674.
35. Richardson, S.D., Lebron, B.L., Miller, C.T., and Aitken, M.D. (2011). Recovery of phenanthrene-degrading bacteria after simulated in situ persulfate oxidation in contaminated soil. Environ. Sci. Technol. 45, 719.
36. Saavedra, J., Acevedo, F., González, M., and Seeger, M. (2010). Mineralization of PCBs by the genetically modified strain Cupriavidus necator JMS34 and its application for bioremediation of PCBs in soil. Appl. Microbiol. Biotechnol. 87, 1543.
37. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J. et al. (2009). Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for describing and comparing microbial communities. Appl Environ Microb. 75, 7537.
38. Shuttleworth, K.L., and Cerniglia, C.E. (1996). Bacterial degradation of low concentrations of phenanthrene and inhibition by naphthalene. Microb. Ecol. 31, 305.
39. Singleton, D.R., Hunt, M., Powell, S.N., Frontera-Suau, R., and Aitken, M.D. (2007). Stable-isotope probing with multiple growth substrates to determine substrate specificity of uncultivated bacteria. J. Microbiol. Methods. 69, 180.
40. Singleton, D.R., Powell, S.N., Sangaiah, R., Gold, A., Ball, L.M., and Aitken, M.D. (2005). Stable-isotope probing of bacteria capable of degrading salicylate, naphthalene or phenanthrene in a bioreactor treating contaminated soil. Appl. Environ. Microbiol. 71, 1202.
41. Singleton, D.R., Richardson, S.D., and Aitken, M.D. (2008). Effects of enrichment with phthalate on polycyclic aromatic hydrocarbon biodegradation in contaminated soil. Biodegradation 19, 577.
42. Singleton, D.R., Richardson, S.D., and Aitken, M.D. (2011). Pyrosequence analysis of bacterial communities in areobic bioreactors treating polycyclic aromatic hydrocarboncontaminated soil. Biodegradation 22, 1061.
43. Singleton, D.R., Sangaiah, R., Gold, A., Ball, L.M., and Aitken, M.D. (2006). Identification and quantification of uncultivated proteobacteria associatedwithpyrene degradationin a bioreactor treating PAH-contaminated soil. Environ. Microbiol. 8, 1736.
44. Stringfellow, W.T., and Aitken, M.D. (1995). Competitive metabolism of naphthalene, methylnaphthalenes, and fluorene by phenanthrene-degrading pseudomonads. Appl. Environ. Microbiol. 61, 357.
45. Suzuki, M.T., and Giovannoni, S.J. (1996). Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl. Environ. Microbiol. 62, 625.
46. USEPA Office of Solid Waste and Emergency Response. (2010). Superfund Remedy Report, Thirteenth Edition. Washington, DC: U.S. Environmental Protection Agency.
47. Vandamme, P., and Coenye, T. (2004). Taxonomy of the genus Cupriavidus: a tale of lost and found. Int. J. Syst. Evol. Microbiol. 54, 2285.
48. Widada, J., Nojiri, H., Kasuga, K., Yoshida, T., Habe, H., and Omori, T. (2002).Molecular detection and diversity of polycyclic aromatic hydrocarbon-degrading bacteria isolated from geographically diverse sites. Appl. Microbiol. Biotechnol. 58, 202.
49. Wilcke, W. (2007). Global patterns of polycyclic aromatic hydrocarbons (PAHs) in soil. Geoderma 141, 157.
50. Zhang, D.-C., Liu, H.-C., Xin, Y.-H., Zhou, Y.-G., Schinner, F., and Margesin, R. (2010). Luteimonas terricola sp. nov., a psychrophilic bacterium isolated from soil. Int. J. Syst. Evol. Microbiol. 60, 1581.
51. Zhao, Z., and Wong, J.W.-C. (2010). Rapid biodegradation of benzo[a]pyrene by Bacillus subtilis BUM under thermophilic condition. Environ. Eng. Sci. 27, 939.
52. Zhou, Y., and Levy, J.I. (2009). Between-airport heterogeneity in air toxics emissions associated with individual cancer risk thresholds and population risks. Environ. Health. 8, 22.
53. Zhu, H., Singleton, D.R., and Aitken, M.D. (2010). Effects of nonionic surfactant addition on populations of polycyclic aromatic hydrocarbon-degrading bacteria in a bioreactor treating contaminated soil. Environ. Sci. Technol. 44, 7266.