Key high molecular weight PAH-degrading bacteria in a soil consortium enriched using a sand-in-liquid microcosm system

Applied Microbiology and Biotechnology

Volumn 100, Issue 7, 2016, Pages 3321-3336

  Tauler, Margalida ^a   Vila, Joaquim ^a   Nieto, José María ^a   Grifoll, Magdalena ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Biodegradation; Microbial community analysis; Microbial consortium; PAHs; Polluted soil

Indexed keywords

ANTHRACENE; AROMATIC HYDROCARBONS; BACTERIA; BIODEGRADATION; MICROORGANISMS; MOLECULAR WEIGHT; PYRENE; SOIL POLLUTION; SOILS;

BENZO[A]ANTHRACENE; GAMMAPROTEOBACTERIA; HIGH MOLECULAR WEIGHT; MICROBIAL COMMUNITIES; MICROBIAL COMMUNITY ANALYSIS; MICROBIAL CONSORTIA; PAH-DEGRADING BACTERIA; POLLUTED SOILS;

POLYCYCLIC AROMATIC HYDROCARBONS;

BENZ[A]ANTHRACENE; CHRYSENE; FLUORANTHENE; PHENANTHRENE; POLYCYCLIC AROMATIC HYDROCARBON; PYRENE; ANTHRACENE DERIVATIVE; PHENANTHRENE DERIVATIVE; PYRENE DERIVATIVE; SOIL; SOIL POLLUTANT;

BACTERIUM; BIODEGRADATION; COMMUNITY COMPOSITION; CREOSOTE; GENE; MICROBIAL COMMUNITY; MICROCOSM; POLLUTANT REMOVAL; PYRENE; SOIL MICROORGANISM; SOIL POLLUTION; WEIGHT;

ACHROMOBACTER; ARTICLE; BACTERIUM; DEGRADATION; METABOLOMICS; MICROBIAL COMMUNITY; MICROBIAL CONSORTIUM; MOLECULAR WEIGHT; MYCOBACTERIUM; NONHUMAN; PSEUDOMONAS; PYROSEQUENCING; SPHINGOBIUM; SPHINGOMONAS; BIOREMEDIATION; CHEMISTRY; CLASSIFICATION; GAMMAPROTEOBACTERIA; GENE LIBRARY; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYLOGENY; SOIL; SOIL POLLUTANT; SPAIN; SPHINGOMONADACEAE;

ACHROMOBACTER; BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; GAMMAPROTEOBACTERIA; MYCOBACTERIUM; PSEUDOMONAS; SPHINGOBIUM; SPHINGOMONAS;

ACHROMOBACTER; ANTHRACENES; BIODEGRADATION, ENVIRONMENTAL; GAMMAPROTEOBACTERIA; GENE LIBRARY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICROBIAL CONSORTIA; MYCOBACTERIUM; PHENANTHRENES; PHYLOGENY; POLYCYCLIC AROMATIC HYDROCARBONS; PSEUDOMONAS; PYRENES; SOIL; SOIL MICROBIOLOGY; SOIL POLLUTANTS; SPAIN; SPHINGOMONADACEAE;

EID: 84960807590     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-7195-8     Document Type: Article

References (58)

1. Bouchez M, Blanchet D, Haeseler F (2000) Efficiency of defined strains and of soil consortia in the biodegradation of polycyclic aromatic hydrocarbon (PAH) mixtures. Biodegradation 10:429–435
2. Buckley DH, Graber JR, Schmidt TM (1998) Phylogenetic analysis of nonthermophilic members of the kingdom Crenarchaeota and their diversity and abundance in soils. Appl Environ Microbiol 64:4333–4339
3. Caldini G, Cenci G, Manenti R, Morozzi G (1995) The ability of an environmental isolate of Pseudomonas fluorescens to utilize chrysene and other four-ring polynuclear aromatic hydrocarbons. Appl Microbiol Biotechnol 44:225–229
4. Cébron A, Norini M-P, 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
5. Dastgheib SMM, Amoozegar MA, Khajeh K, Shavandi M, Ventosa A (2012) Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Appl Microbiol Biotechnol 95:789–798
6. DeBruyn JM, Mead TJ, Sayler GS (2012) Horizontal transfer of PAH catabolism genes in Mycobacterium: evidence from comparative genomics and isolated pyrene-degrading bacteria. Environ Sci Technol 46:99–106
7. Edwards SJ, Kjellerup BV (2013) Applications of biofilms in bioremediation and biotransformation of persistent organic pollutants, pharmaceuticals/personal care products, and heavy metals. Appl Microbiol Biotechnol 97:9909–9921
8. El Fantroussi S, Verschuere L, Verstraete W, Top EM (1999) Effect of phenylurea herbicides on soil microbial communities estimated by analysis of 16S rRNA gene fingerprints and community-level physiological profiles. Appl Environ Microbiol 65:982–988
9. Ferrero M, Llobet-Brossa E, Lalucat J, García-Valdés E, Rosselló-Móra R, Bosch R (2002) Coexistence of two distinct copies of naphthalene degradation genes in Pseudomonas strains isolated from the western Mediterranean region. Appl Environ Microbiol 68:957–962
10. Gallego S, Vila J, Tauler M, Nieto JM, Breugelmans P, Springael D, Grifoll M (2014) Community structure and PAH ring-hydroxylating dioxygenase genes of a marine pyrene-degrading microbial consortium. Biodegradation 25:543–556
11. Gillespie IMM, Philp JC (2013) Bioremediation, an environmental remediation technology for the bioeconomy. Trends Biotechnol 31:329–332
12. Grifoll M, Selifonov S, Gatlin CV, Chapman PJ (1995) Actions of a versatile fluorene-degrading bacterial isolate on polycyclic aromatic compounds. Appl Environ Microbiol 61:3711–3723
13. Hamaki T, Suzuki M, Fudou R, Jojima Y, Kajiura T, Tabuchi A, Sen K, Shibai H (2005) Isolation of novel bacteria and actinomycetes using soil-extract agar medium. J Biosci Bioeng 99:485–492
14. Heuer H, Krsek M, Baker P, Smalla K, Wellington EM (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241
15. Iwai S, Johnson T, Chai B, Hashsham S, Tiedje JM (2011) Comparison of the specificities and efficacies of primers for aromatic dioxygenase gene analysis of environmental samples. Appl Environ Microbiol 77:3551–3557
16. Jones M, Rodgers-Vieira E, Hu J, Aitken MD (2014) Association of growth substrates and bacterial genera with benzo[a]pyrene mineralization in contaminated soil. Environ Eng Sci 31:689–697
17. Jones MD, Crandell DW, Singleton DR, Aitken MD (2011) Stable-isotope probing of the polycyclic aromatic hydrocarbon-degrading bacterial guild in a contaminated soil. Environ Microbiol 13:2623–2632
18. 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
19. Kanaly RA, Harayama S (2010) Advances in the field of high-molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microb Biotechnol 3:136–164
20. Kanaly RA, Bartha R, Watanabe K, Harayama S (2000) Rapid mineralization of benzo[a]pyrene by a microbial consortium growing on diesel fuel. Appl Environ Microbiol 66:4205–4211
21. Khara P, Roy M, Chakraborty J, Ghosal D, Dutta TK (2014) Functional characterization of diverse ring-hydroxylating oxygenases and induction of complex aromatic catabolic gene clusters in Sphingobium sp. PNB. FEBS Open Bio 4:290–300
22. Kohlmeier S, Smits THM, Ford RM, Keel C, Harms H, Wick LY (2005) Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol 39:4640–4646
23. Kostka JE, Prakash O, Overholt W, Green SJ, Freyer G, Canion A, Delgardio J, Norton N, Hazen TC, Huettel M (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the deepwater horizon oil spill. Appl Environ Microbiol 77:7962–7974
24. Kunihiro M, Ozeki Y, Nogi Y, Hamamura N, Kanaly RA (2013) Benz[a]anthracene biotransformation and production of ring fission products by Sphingobium sp. strain KK22. Appl Environ Microbiol 79:4410–4420
25. Kweon O, Kim S-J, Freeman JP, Song J, Baek S, Cerniglia CE (2010) Substrate specificity and structural characteristics of the novel Rieske nonheme iron aromatic ring-hydroxylating oxygenases NidAB and NidA3B3 from Mycobacterium vanbaalenii PYR-1. MBio 1(2):e00135–e00110
26. Kweon O, Kim S-J, Kim DW, Kim JM, Kim H-L, Ahn Y, Sutherland JB, Cerniglia CE (2014) Pleiotropic and epistatic behavior of a ring-hydroxylating oxygenase system in the polycyclic aromatic hydrocarbon metabolic network from Mycobacterium vanbaalenii PYR-1. J Bacteriol 196:3503–3515
27. Lafortune I, Juteau P, Déziel E, Lépine F, Beaudet R, Villemur R (2009) Bacterial diversity of a consortium degrading high-molecular-weight polycyclic aromatic hydrocarbons in a two-liquid phase biosystem. Microb Ecol 57:455–468
28. Leys NM, Bastiaens L, Verstraete W, Springael D (2005a) Influence of the carbon/nitrogen/phosphorus ratio on polycyclic aromatic hydrocarbon degradation by Mycobacterium and Sphingomonas in soil. Appl Microbiol Biotechnol 66:726–736
29. Leys NM, Ryngaert A, Bastiaens L, Wattiau P, Top EM, Verstraete W, Springael D (2005b) Occurrence and community composition of fast-growing Mycobacterium in soils contaminated with polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol 51:375–388
30. Leys NMEJ, Ryngaert A, Bastiaens L, Verstraete W, Top EM, Springael D (2004) Occurrence and phylogenetic diversity of Sphingomonas strains in soils contaminated with polycyclic aromatic hydrocarbons. Appl Environ Microbiol 70:1944–1955
31. van Liedekerke M, Prokop G, Rabl-berger S, Kibblewhite M (2014) Progress in the management of contaminated sites in Europe. In: JRC Reference Reports Report EUR 26376 EN
32. Lladó S, Gràcia E, Solanas AM, Viñas M (2013) Fungal and bacterial microbial community assessment during bioremediation assays in an aged creosote-polluted soil. Soil Biol Biochem 67:114–123
33. López Z, Vila J, Grifoll M (2005) Metabolism of fluoranthene by mycobacterial strains isolated by their ability to grow in fluoranthene or pyrene. J Ind Microbiol Biotechnol 32:455–464
34. López Z, Vila J, Minguillón C, Grifoll M (2006) Metabolism of fluoranthene by Mycobacterium sp. strain AP1. Appl Microbiol Biotechnol 70:747–756
35. López Z, Vila J, Ortega-Calvo JJ, Grifoll M (2008) Simultaneous biodegradation of creosote-polycyclic aromatic hydrocarbons by a pyrene-degrading Mycobacterium. Appl Microbiol Biotechnol 78:739–739
36. Martin F, Torelli S, Le Paslier D, Barbance A, Martin-Laurent F, Bru D, Geremia R, Blake G, Jouanneau Y (2012) Betaproteobacteria dominance and diversity shifts in the bacterial community of a PAH-contaminated soil exposed to phenanthrene. Environ Pollut 162:345–353
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
38. Mueller JG, Chapman PJ, Blattmann BO, Pritchard PH (1990) Isolation and characterization of a fluoranthene-utilizing strain of Pseudomonas paucimobilis. Appl Environ Microbiol 56:1079–1086
39. Ortega-Calvo JJ, Birman I, Alexander M (1995) Effect of varying the rate of partitioning of phenanthrene in nonaqueous-phase liquids on biodegradation in soil slurries. Environ Sci Technol 29:2222–2225
40. Peng R-H, Xiong A-S, Xue Y, Fu X-Y, Gao F, Zhao W, Tian Y-S, Yao Q-H (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955
41. Prince RC, Elmendorf DL, Lute JR, Hsu CS, Halth CE, Senius JD, Dechert GJ, Douglas GS, Butler EL (1994) 17α(H),21β(H)-hopane as a conserved internal marker for estimating the biodegradation of crude oil. Environ Sci Technol 28:142–145
42. Roy M, Khara P, Dutta TK (2012) Meta-cleavage of hydroxynaphthoic acids in the degradation of phenanthrene by Sphingobium sp. strain PNB. Microbiology 158:685–695
43. Schuler L, Jouanneau Y, Chadhain SMN, Meyer C, Pouli M, Zylstra GJ, Hols P, Agathos SN (2009) Characterization of a ring-hydroxylating dioxygenase from phenanthrene-degrading Sphingomonas sp. strain LH128 able to oxidize benz[a]anthracene. Appl Microbiol Biotechnol 83:465–475
44. 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
45. Sohn JH, Kwon KK, Kang J-H, Jung H-B, Kim S-J (2004) Novosphingobium pentaromativorans sp. nov., a high-molecular-mass polycyclic aromatic hydrocarbon-degrading bacterium isolated from estuarine sediment. Int J Syst Evol Microbiol 54:1483–1487
46. Stolz A (2009) Molecular characteristics of xenobiotic-degrading sphingomonads. Appl Microbiol Biotechnol 81:793–811
47. Sun R, Jin J, Sun G, Liu Y, Liu Z (2010) Screening and degrading characteristics and community structure of a high molecular weight polycyclic aromatic hydrocarbon-degrading bacterial consortium from contaminated soil. J Environ Sci 22:1576–1585
48. Vanbroekhoven K, Ryngaert A, Bastiaens L, Wattiau P, Vancanneyt M, Swings J, De Mot R, Springael D (2004) Streptomycin as a selective agent to facilitate recovery and isolation of introduced and indigenous Sphingomonas from environmental samples. Environ Microbiol 6:1123–1136
49. Vila J, Grifoll M (2009) Actions of Mycobacterium sp. strain AP1 on the saturated- and aromatic-hydrocarbon fractions of fuel oil in a marine medium. Appl Environ Microbiol 75:6232–6239
50. Vila J, López Z, Sabaté J, Minguillón C, Solanas AM, Grifoll M (2001) Identification of a novel metabolite in the degradation of pyrene by Mycobacterium sp. strain AP1: actions of the isolate on two- and three-ring polycyclic aromatic hydrocarbons. Appl Environ Microbiol 67:5497–5505
51. Vila J, Tauler M, Grifoll M (2015) Bacterial PAH degradation in marine and terrestrial habitats. Curr Opin Biotechnol 33:95–102
52. Viñas M, Sabaté J, Espuny MJ, Solanas AM (2005) Bacterial community dynamics and polycyclic aromatic hydrocarbon degradation during bioremediation of heavily creosote-contaminated soil. Appl Environ Microbiol 71:7008–7018
53. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
54. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
55. Weissenfels WD, Beyer M, Klein J (1990) Degradation of phenanthrene, fluorene and fluoranthene by pure bacterial cultures. Appl Microbiol Biotechnol 32:479–484
56. Wrenn BA, Venosa AD (1996) Selective enumeration of aromatic and aliphatic hydrocarbon degrading bacteria by a most-probable-number procedure. Can J Microbiol 42:252–258
57. Wright ES, Yilmaz LS, Noguera DR (2012) DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl Environ Microbiol 78:717–725
58. Yabuuchi E, Kawamura Y, Kosako Y, Ezaki T (1998) Emendation of genus Achromobacter and Achromobacter xylosoxidans (Yabuuchi and Yano) and proposal of Achromobacter ruhlandii (Packer and Vishniac) comb. nov., Achromobacter piechaudii (Kiredjian et al.) comb. nov., and Achromobacter xylosoxidans subsp. denitrificans (Rüger and Tan) comb. nov. Microbiol Immunol 42:429–438