Identification of Benzo[a]pyrene-metabolizing bacteria in forest soils by using DNA-based stable-isotope probing

Applied and Environmental Microbiology

Volumn 81, Issue 21, 2015, Pages 7368-7376

  Song, Mengke ^a   Luo, Chunling ^a   Jiang, Longfei ^a   Zhang, Dayi ^b   Wang, Yujie ^c   Zhang, Gan ^a  

^a GUANGZHOU INSTITUTE OF GEOCHEMISTRY   (China)

^b LANCASTER UNIVERSITY   (United Kingdom)

^c GUANGDONG UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBONS; BIOREMEDIATION; DEGRADATION; DNA; FORESTRY; ISOTOPES; METABOLISM; MICROBIOLOGY; MICROORGANISMS; NATURAL ATTENUATION; PHYSIOLOGY; POLYCYCLIC AROMATIC HYDROCARBONS; PYRENE; SOIL POLLUTION; SOILS;

ADDITIVE EFFECTS; CONTAMINATED SOILS; DEGRADATION EFFICIENCY; DIFFERENT SOILS; MICROBIAL DIVERSITY; SOIL MICROCOSMS; STABLE-ISOTOPE PROBING; UNCULTIVATED BACTERIA;

BACTERIA;

AROMATIC HYDROCARBON; BACTERIUM; BIODEGRADATION; BIOREMEDIATION; DNA; FOREST SOIL; GENE EXPRESSION; IDENTIFICATION METHOD; ISOTOPIC ANALYSIS; METABOLISM; MICROBIAL COMMUNITY; MICROCOSM; MOUNTAIN; STABLE ISOTOPE;

CHINA; HEILONGJIANG; HUBEI;

BACTERIA (MICROORGANISMS); BURKHOLDERIA; OXALOBACTERACEAE; SPHINGOBACTERIALES;

BACTERIAL DNA; BENZO[A]PYRENE; DIOXYGENASE;

BACTEROIDETES; BURKHOLDERIA; CHEMISTRY; CHINA; CLASSIFICATION; DNA SEQUENCE; FOREST; GENETICS; ISOTOPE LABELING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; OXALOBACTERACEAE; POLYMERASE CHAIN REACTION;

BACTEROIDETES; BENZO(A)PYRENE; BURKHOLDERIA; CHINA; DIOXYGENASES; DNA, BACTERIAL; FORESTS; ISOTOPE LABELING; MOLECULAR SEQUENCE DATA; OXALOBACTERACEAE; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY;

EID: 84944401755     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01983-15     Document Type: Article

References (60)

1. Baek SO, Field RA, Goldstone ME, Kirk PW, Lester JN, Perry R. 1991. A Review of atmospheric polycyclic aromatic-hydrocarbons-sources, fate and behavior. Water Air Soil Pollut 60:279-300. http://dx.doi.org/10.1007/BF00282628.
2. Zhang YX, Tao S. 2009. Global atmospheric emission inventory of polycyclic aromatic hydrocarbons (PAHs) for 2004. Atmos Environ 43:812-819. http://dx.doi.org/10.1016/j.atmosenv.2008.10.050.
3. Keith LH, Telliard WA. 1979. Priority pollutants I-a perspective view. Environ Sci Technol 13:416-423. http://dx.doi.org/10.1021/es60152a601.
4. Rodríguez-Fragoso L, Melendez K, Hudson LG, Lauer FT, Burchiel SW. 2009. EGF-receptor phosphorylation and downstream signaling are activated by benzo[a]pyrene 3,6-quinone and benzo[a]pyrene 1,6-quinone in human mammary epithelial cells. Toxicol Appl Pharmacol 235:321-328. http://dx.doi.org/10.1016/j.taap.2008.12.022.
5. Wills LP, Zhu SQ, Willett KL, Di Giulio RT. 2009. Effect of CYP1A inhibition on the biotransformation of benzo[a]pyrene in two populations of Fundulus heteroclitus with different exposure histories. Aquat Toxicol 92:195-201. http://dx.doi.org/10.1016/j.aquatox.2009.01.009.
6. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. 2010. Household use of solid fuels and high-temperature frying. IARC Monogr Eval Carcinog Risks Hum 95:9-38.
7. Juhasz AL, Naidu R. 2000. Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegradation 45:57-88. http://dx.doi.org/10.1016/S0964-8305(00)00052-4.
8. Rentz JA, Alvarez PJJ, Schnoor JL. 2008. Benzo[a]pyrene degradation by Sphingomonas yanoikuyae JAR02. Environ Pollut 151:669-677. http://dx.doi.org/10.1016/j.envpol.2007.02.018.
9. Peng H, Yin H, Deng J, Ye JS, Chen SN, He BY, Zhang N. 2012. Biodegradation of benzo[a]pyrene by Arthrobacter oxydans B4. Pedosphere 22:554-561. http://dx.doi.org/10.1016/S1002-0160(12)60040-X.
10. Mishra S, Singh SN. 2014. Biodegradation of benzo(a)pyrene mediated by catabolic enzymes of bacteria. Int J Environ Sci Technol (Tehran) 11: 1571-1580. http://dx.doi.org/10.1007/s13762-013-0300-6.
11. Jurelevicius D, Alvarez VM, Peixoto R, Rosado AS, Seldin L. 2012. Bacterial polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenases (PAH-RHD) encoding genes in different soils from King George Bay, Antarctic Peninsula. Appl Soil Ecol 55:1-9. http://dx.doi.org/10.1016/j.apsoil.2011.12.008.
12. Cébron A, Norini MP, Beguiristain T, Leyval C. 2008. Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHD alpha) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Methods 73:148-159. http://dx.doi.org/10.1016/j.mimet.2008.01.009.
13. Lily MK, Bahuguna A, Dangwal K, Garg V. 2009. Degradation of benzo [a] pyrene by a novel strain Bacillus subtilis Bmt4i (Mtcc 9447). Braz J Microbiol 40:884-892. http://dx.doi.org/10.1590/S1517-83822009000400020.
14. Kanaly RA, Harayama S. 2000. Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059-2067. http://dx.doi.org/10.1128/JB.182.8.2059-2067.2000.
15. Kanaly RA, Harayama S. 2010. Advances in the field of high-molecularweight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microb Biotechnol 3:136-164. http://dx.doi.org/10.1111/j.1751-7915.2009.00130.x.
16. Chen SH, Aitken MD. 1999. Salicylate stimulates the degradation of high molecular weight polycyclic aromatic hydrocarbons by Pseudomonas saccharophila P15. Environ Sci Technol 33:435-439. http://dx.doi.org/10.1021/es9805730.
17. Alemayehu D, Gordon LM, O'Mahony MM, O'Leary ND, Dobson ADW. 2004. Cloning and functional analysis gene involved in indigo production by gene disruption of a novel and fluoranthene metabolism in Pseudomonas alcaligenes PA-10. FEMS Microbiol Lett 239:285-293. http://dx.doi.org/10.1016/j.femsle.2004.08.046.
18. Bode HB, Muller R. 2005. The impact of bacterial genomics on natural product research. Angew Chem Int Ed 44:6828-6846. http://dx.doi.org/10.1002/anie.200501080.
19. Galvão TC, Mohn WW, de Lorenzo V. 2005. Exploring the microbial biodegradation and biotransformation gene pool. Trends Biotechnol 23: 497-506. http://dx.doi.org/10.1016/j.tibtech.2005.08.002.
20. Lorenz P, Eck J. 2005. Metagenomics and industrial applications. Nat Rev Microbiol 3:510-516. http://dx.doi.org/10.1038/nrmicro1161.
21. Oren A. 2004. Prokaryote diversity and taxonomy: current status and future challenges. Philos Trans R Soc Lond B Biol Sci. 359:623-638. http://dx.doi.org/10.1098/rstb.2003.1458.
22. Radajewski S, Ineson P, Parekh NR, Murrell JC. 2000. Stable-isotope probing as a tool in microbial ecology. Nature 403:646-649. http://dx.doi.org/10.1038/35001054.
23. Singleton DR, Sangaiah R, Gold A, Ball LM, Aitken MD. 2006. Identification and quantification of uncultivated Proteobacteria associated with pyrene degradation in a bioreactor treating PAH-contaminated soil. Environ Microbiol 8:1736-1745. http://dx.doi.org/10.1111/j.1462-2920.2006.01112.x.
24. Luo CL, Xie SG, Sun WM, Li XD, Cupples AM. 2009. Identification of a novel toluene-degrading bacterium from the candidate phylum TM7, as determined by DNA stable isotope probing. Appl Environ Microbiol 75: 4644-4647. http://dx.doi.org/10.1128/AEM.00283-09.
25. Gutierrez T, Singleton DR, Aitken MD, Semple KT. 2011. Stable isotope probing of an algal bloom to identify uncultivated members of the Rhodobacteraceae associated with low-molecular-weight polycyclic aromatic hydrocarbon degradation. Appl Environ Microbiol 77:7856-7860. http://dx.doi.org/10.1128/AEM.06200-11.
26. Singleton DR, Powell SN, Sangaiah R, Gold A, Ball LM, Aitken MD. 2005. Stable-isotope probing of bacteria capable of degrading salicylate, naphthalene, or phenanthrene in a bioreactor treating contaminated soil. Appl Environ Microbiol 71:1202-1209. http://dx.doi.org/10.1128/AEM.71.3.1202-1209.2005.
27. Zhang SY, Wang QF, Xie SG. 2012. Stable isotope probing identifies anthracene degraders under methanogenic conditions. Biodegradation 23:221-230. http://dx.doi.org/10.1007/s10532-011-9501-1.
28. Peng JJ, Zhang Y, Su JQ, Qiu QF, Jia ZJ, Zhu YG. 2013. Bacterial communities predominant in the degradation of C-13(4)-4,5,9,10-pyrene during composting. Bioresour Technol 143:608-614. http://dx.doi.org/10.1016/j.biortech.2013.06.039.
29. Jones MD, Crandell DW, Singleton DR, Aitken MD. 2011. Stableisotope probing of the polycyclic aromatic hydrocarbon-degrading bacterial guild in a contaminated soil. Environ Microbiol 13:2623-2632. http://dx.doi.org/10.1111/j.1462-2920.2011.02501.x.
30. Sul WJ, Park J, Quensen JF, Rodrigues JLM, Seliger L, Tsoi TV, Zylstra GJ, Tiedje JM. 2009. DNA-stable isotope probing integrated with metagenomics for retrieval of biphenyl dioxygenase genes from polychlorinated biphenyl-contaminated river sediment. Appl Environ Microbiol 75: 5501-5506. http://dx.doi.org/10.1128/AEM.00121-09.
31. Uhlik O, Wald J, Strejcek M, Musilova L, Ridl J, Hroudova M, Vlcek C, Cardenas E, Mackova M, Macek T. 2012. Identification of bacteria utilizing biphenyl, benzoate, and naphthalene in long-term contaminated soil. PLoS One 7(7):e40653. http://dx.doi.org/10.1371/journal.pone.0040653.
32. Mu DY, Scow KM. 1994. Effect of trichloroethylene (Tce) and toluene concentrations on Tce and toluene biodegradation and the population density of Tce and toluene degraders in soil. Appl Environ Microbiol 60:2661-2665.
33. Sun WM, Xie SG, Luo CL, Cupples AM. 2010. Direct link between toluene degradation in contaminated-site microcosms and a Polaromonas strain. Appl Environ Microbiol 76:956-959. http://dx.doi.org/10.1128/AEM.01364-09.
34. Cupples AM, Sims GK. 2007. Identification of in situ 2,4-dichlorophenoxyacetic acid-degrading soil microorganisms using DNA-stable isotope probing. Soil Biol Biochem 39:232-238. http://dx.doi.org/10.1016/j.soilbio.2006.07.011.
35. Sun WM, Cupples AM. 2012. Diversity of five anaerobic toluenedegrading microbial communities investigated using stable isotope probing. Appl Environ Microbiol 78:972-980. http://dx.doi.org/10.1128/AEM.06770-11.
36. Warshawsky D, Ladow K, Schneider J. 2007. Enhanced degradation of benzo[a]pyrene by Mycobacterium sp in conjunction with green alga. Chemosphere 69:500-506. http://dx.doi.org/10.1016/j.chemosphere.2007.03.031.
37. Moody JD, Freeman JP, Fu PP, Cerniglia CE. 2004. Degradation of benzo[a]pyrene by Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 70:340-345. http://dx.doi.org/10.1128/AEM.70.1.340-345.2004.
38. Powell SN, Singleton DR, Aitken MD. 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 42:4099-4105. http://dx.doi.org/10.1021/es703007n.
39. Ang EL, Zhao HM, Obbard JP. 2005. Recent advances in the bioremediation of persistent organic pollutants via biomolecular engineering. Enzyme Microb Technol 37:487-496. http://dx.doi.org/10.1016/j.enzmictec.2004.07.024.
40. de Carcer DA, Martin M, Karlson U, Rivilla R. 2007. Changes in bacterial populations and in biphenyl dioxygenase gene diversity in a polychlorinated biphenyl-polluted soil after introduction of willow trees for rhizoremediation. Appl Environ Microbiol 73:6224-6232. http://dx.doi.org/10.1128/AEM.01254-07.
41. Huang X, Luo Y, Hu Z, Tian Y. 2006. Recent advance in the study of persistent organic pollutants bioremediation. Acta Sci Circum 26:353-361.
42. Juhasz AL, Britz ML, Stanley GA. 1997. Degradation of benzo[a]pyrene, dibenz[a,h]anthracene and coronene by Burkholderia cepacia. Water Sci Technol 36:45-51.
43. Zafra G, Absalon AE, Cuevas MD, Cortes-Espinosa DV. 2014. Isolation and selection of a highly tolerant microbial consortium with potential for PAH biodegradation from heavy crude oil-contaminated soils. Water Air Soil Pollut 225:1826. http://dx.doi.org/10.1007/s11270-013-1826-4.
44. Yoon MH, Im WT. 2007. Flavisolibacter ginsengiterrae gen. nov., sp nov and Flavisolibacter ginsengisoli sp nov., isolated from ginseng cultivating soil. Int J Syst Evol Microbiol 57:1834-1839. http://dx.doi.org/10.1099/ijs.0.65011-0.
45. Ye DY, Siddiqi MA, Maccubbin AE, Kumar S, Sikka HC. 1996. Degradation of polynuclear aromatic hydrocarbons by Sphingomonas paucimobilis. Environ Sci Technol 30:136-142. http://dx.doi.org/10.1021/es9501878.
46. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, Possemiers S, Van Holle A, Francois P, de Vos WM, Delzenne NM, Schrenzel J, Cani PD. 2011. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60:3307-3307. http://dx.doi.org/10.2337/db11-er12c.
47. Chang H, Nie M, Ge B, Liu C, Yang Q, Zhou L, Fan X, Sun C. 2013. Effects of rhamnolipid on oil degradation by Pseudomonas aeruginosa strain NY3. Chin J Environ Eng 7:771-776.
48. Tejeda-Agredano MC, Gallego S, Vila J, Grifoll M, Ortega-Calvo JJ, Cantos M. 2013. Influence of the sunflower rhizosphere on the biodegradation of PAHs in soil. Soil Biol Biochem 57:830-840. http://dx.doi.org/10.1016/j.soilbio.2012.08.008.
49. Habe H, Omori T. 2003. Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67: 225-243. http://dx.doi.org/10.1271/bbb.67.225.
50. Herrick JB, Stuart-Keil KG, Ghiorse WC, Madsen EL. 1997. Natural horizontal transfer of a naphthalene dioxygenase gene between bacteria native to a coal tar-contaminated field site. Appl Environ Microbiol 63: 2330-2337.
51. Wilson MS, Herrick JB, Jeon CO, Hinman DE, Madsen EL. 2003. Horizontal transfer of phnAc dioxygenase genes within one of two phenotypically and genotypically distinctive naphthalene-degrading guilds from adjacent soil environments. Appl Environ Microbiol 69:2172-2181. http://dx.doi.org/10.1128/AEM.69.4.2172-2181.2003.
52. Yagi JM, Sims D, Brettin T, Bruce D, Madsen EL. 2009. The genome of Polaromonas naphthalenivorans strain CJ2, isolated from coal tarcontaminated sediment, reveals physiological and metabolic versatility and evolution through extensive horizontal gene transfer. Environ Microbiol 11:2253-2270. http://dx.doi.org/10.1111/j.1462-2920.2009.01947.x.
53. Trieu-Cuot P, Gerbaud G, Lambert T, Courvalin P. 1985. In vivo transfer of genetic information between gram-positive and gram-negative bacteria. EMBO J 4:3583-3587.
54. Zhang DY, Berry JP, Zhu D, Wang Y, Chen Y, Jiang B, Huang S, Langford H, Li GH, Davison PA, Xu J, Aries E, Huang WE. 2015. Magnetic nanoparticle-mediated isolation of functional bacteria in a complex microbial community. ISME J 9:603-614. http://dx.doi.org/10.1038/ismej.2014.161.
55. Kästner M, Breuer-Jammali M, Mahro B. 1998. Impact of inoculation protocols, salinity, and pH on the degradation of polycyclic aromatic hydrocarbons (PAHs) and survival of PAH-degrading bacteria introduced into soil. Appl Environ Microbiol 64:359-362.
56. Wong JWC, Lai KM, Wan CK, Ma KK, Fang M. 2002. Isolation and optimization of PAH-degradative bacteria from contaminated soil for PAHs bioremediation. Water Air Soil Pollut 139:1-13. http://dx.doi.org/10.1023/A:1015883924901.
57. Ogunseitan OA, Delgado IL, Tsai YL, Olson BH. 1991. Effect of 2-hydroxybenzoate on the maintenance of naphthalene-degrading pseudomonads in seeded and unseeded soil. Appl Environ Microbiol 57:2873-2879.
58. Ogunseitan OA, Olson BH. 1993. Effect of 2-hydroxybenzoate on the rate of naphthalene mineralization in soil. Appl Microbiol Biot 38:799-807. http://dx.doi.org/10.1007/BF00167148.
59. Ji PS, Wilson M. 2003. Enhancement of population size of a biological control agent and efficacy in control of bacterial speck of tomato through salicylate and ammonium sulfate amendments. Appl Environ Microbiol 69:1290-1294. http://dx.doi.org/10.1128/AEM.69.2.1290-1294.2003.
60. Carmichael LM, Pfaender FK. 1997. The effect of inorganic and organic supplements on the microbial degradation of phenanthrene and pyrene in soils. Biodegradation 8:1-13. http://dx.doi.org/10.1023/A:1008258720649.