Variovorax sp.-mediated biodegradation of the phenyl urea herbicide linuron at micropollutant concentrations and effects of natural dissolved organic matter as supplementary carbon source

Applied Microbiology and Biotechnology

Volumn 97, Issue 22, 2013, Pages 9837-9846

  Horemans, Benjamin ^a   Vandermaesen, Johanna ^a   Vanhaecke, Lynn ^b   Smolders, Erik ^a   Springael, Dirk ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Biodegradation; Dissolved organic matter; Linuron; Micropollutants; Variovorax

Indexed keywords

BIODEGRADABLE COMPOUNDS; DEGRADATION OF POLLUTANTS; DISSOLVED ORGANIC MATTERS; INITIAL CONCENTRATION; LINURON; MICROPOLLUTANTS; POLLUTANT-DEGRADING BACTERIA; VARIOVORAX;

BIOLOGICAL MATERIALS; CARBON; DEGRADATION; MICROBIOLOGY; PESTICIDES; UREA;

BIODEGRADATION;

CITRIC ACID; DISSOLVED ORGANIC MATTER; LINURON; ORGANIC CARBON; PESTICIDE;

BACTERIUM; BIODEGRADATION; CARBON; DISSOLVED ORGANIC MATTER; GROWTH RATE; HETEROTROPHY; INHIBITION; LINURON;

ARTICLE; BACTERIAL STRAIN; BACTERIUM; BACTERIUM CULTURE; BIODEGRADABILITY; BIODEGRADATION; CARBON SOURCE; DEGRADATION KINETICS; MICROBIAL CONSORTIUM; NONHUMAN; POLLUTANT; VARIOVORAX;

BACTERIA (MICROORGANISMS); VARIOVORAX;

BIOTRANSFORMATION; CARBON; COMAMONADACEAE; ENVIRONMENTAL POLLUTANTS; HERBICIDES; LINURON;

EID: 84888428006     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-4690-7     Document Type: Article

References (41)

1. Alexander M (1981) Biodegradation of chemicals of environmental concern. Science 211:132-138. doi: 10.1126/science.7444456
2. Bally M, Egli T (1996) Dynamics of substrate consumption and enzyme synthesis in Chelatobacter heintzii during growth in carbon-limited continuous culture with different mixtures of glucose and nitrilotriacetate. Appl Environ Microbiol 62:133-140
3. Bers K, Sniegowski K, De Mot R, Springael D (2012) Dynamics of the linuron hydrolase libA gene pool size in response to linuron application and environmental perturbations in agricultural soil and on-farm biopurification systems. Appl Environ Microbiol 78:2783-2789. doi: 10.1128/aem.06991-11
4. Bers K, Leroy B, Breugelmans P, Albers P, Lavigne R, Sørensen S, Springael D (2011) A novel linuron hydrolase identified by genomic-proteomic analysis of phenylurea herbicide mineralization by Variovorax sp. strain SRS16. Appl Environ Microbiol 78. doi: 10.1128/AEM.06162-11
5. Breugelmans P, D'Huys P-J, De Mot R, Springael D (2007) Characterization of novel linuron-mineralizing bacterial consortia enriched from long-term linuron-treated agricultural soils. FEMS Microbiol Ecol 62:374-385. doi: 10.1111/j.1574-6941.2007.00391.x
6. Breugelmans P, Barken KB, Tolker-Nielsen T, Hofkens J, Dejonghe W, Springael D (2008) Architecture and spatial organization in a triple-species bacterial biofilm synergistically degrading the phenylurea herbicide linuron. FEMS Microbiol Ecol 64:271-282. doi: 10.1111/j.1574-6941.2008.00470.x
7. Buekers J (2007) Fixation of cadmium, copper, nickel and zinc in soil: kinetics, mechanism and its effect on metal bioavailability. Dissertation, Catholic University of Leuven, Leuven, Belgium
8. Caux PY, Kent RA, Fan GT, Grande C (1998) Canadian water quality guidelines for linuron. Environ Toxicol and Water Quality 13:1-41. doi:10.1002/(sici)1098-2256(1998) 13:1<1::aid-tox1>3.0.co;2-b
9. Chiou CT, Malcolm RL, Brinton TI, Kile DE (1986) Water solubility enhancement of some organic pollutants and pesticides by dissolved humic and fulvic acids. Environ Sci & Tech 20:502-508. doi: 10.1021/es00147a010
10. Copley S (2000) Evolution of a metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach. Trends Biochem Sci 25:261-265. doi: 10.1016/S0968-0004(00)01562-0
11. Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 107:907-938. doi: 10.1016/j.envpol.2005.12.018
12. de Lipthay JR, Sørensen SR, Aamand J (2007) Effect of herbicide concentration and organic and inorganic nutrient amendment on the mineralization of mecoprop, 2,4-D and 2,4,5-T in soil and aquifer samples. Environ Pollut 148:83-93. doi: 10.1016/j.envpol.2006.11.005
13. Dejonghe W, Berteloot E, Goris J, Boon N, Crul K, Maertens S, Höfte M, Vos PD, Verstraete W, Top EM (2003) Synergistic degradation of linuron by a bacterial consortium and isolation of a single linuron-degrading Variovorax strain. Appl Environ Microbiol 69:1532-1541. doi: 10.1128/AEM.69.3.1532-1541. 2003
14. Delle Site A (2001) Factors affecting sorption of organic compounds in natural sorbent/water systems and sorption coefficients for selected pollutants. A review. J Phys Chem Ref Data 30:187-439
15. EU (1998) Council Directive 98/83/EC of 3 November 1998 on the quality of water intended for human consumption. Council of the European Union
16. Hess TF, Schmidt SK, Silverstein J, Howe B (1990) Supplemental substrate enhancement of 2,4-dinitrophenol mineralization by a bacterial consortium. Appl Environ Microbiol 56:1551-1558
17. Horemans B, Smolders E, Springael D (2012a) Carbon source utilization profiles suggest additional metabolic interactions in a synergistic linuron degrading bacterial consortium. FEMS Microbiol Ecol. doi: 10.1111/1574-6941. 12033
18. Horemans B, Vandermaesen J, Smolders E, Springael D (2012b) Cooperative dissolved organic carbon assimilation by a linuron degrading bacterial consortium. FEMS Microbiol Ecol. doi: 10.1111/1574-6941.12036
19. Iglesias-Jiménez E, Poveda E, Sánchez-Martín MJ, Sánchez-Camazano M (1997) Effect of the nature of exogenous organic matter on pesticide sorption by the soil. Archives of Environ Contamination and Toxicol 33:117-124. doi: 10.1007/s002449900232
20. Keuth S, Rehm H-J (1991) Biodegradation of phenanthrene by Arthrobacter polychromogenes isolated from a contaminated soil. Appl Microbiol Biotechnol 34:804-808. doi: 10.1007/bf00169354
21. Kovárová-kovar K, Egli T (1998) Growth kinetics of suspended microbial cells: from single-substrate-controlled growth to mixed-substrate kinetics. Microbiol Mol Biol Rev 62:646-666
22. Larsson P, Okla L, Tranvik L (1988) Microbial degradation of xenobiotic, aromatic pollutants in humic water. Appl Environ Microbiol 54:1864-1867
23. Levesque M, Schnitzer M (1967) The extraction of soil organic matter by base and chelating resin. Can J Soil Sci 25:47-51. doi: 10.4141/cjss67-012
24. McFall SM, Abraham B, Narsolis CG, Chakrabarty AM (1997) A tricarboxylic acid cycle intermediate regulating transcription of a chloroaromatic biodegradative pathway: fumarate-mediated repression of the clcABD operon. J Bacteriol 179:6729-6735
25. Müller C, Petruschka L, Cuypers H, Burchhardt G, Herrmann H (1996) Carbon catabolite repression of phenol degradation in Pseudomonas putida is mediated by the inhibition of the activator protein PhlR. J Bacteriol 178:2030-2036
26. Ortega-Calvo JJ, Saiz-Jimenez C (1998) Effect of humic fractions and clay on biodegradation of phenanthrene by a Pseudomonas fluorescens strain isolated from soil. Appl Environ Microbiol 64:3123-3126
27. Rapp P, Timmis KN (1999) Degradation of chlorobenzenes at nanomolar concentrations by Burkholderia sp. strain PS14 in liquid cultures and in soil. Appl Environ Microbiol 65:2547-2552
28. Rentz JA, Alvarez PJJ, Schnoor JL (2004) Repression of Pseudomonas putida phenanthrene degrading activity by plant root extracts and exudates. Environ Microbiol 6:574-583. doi: 10.1111/j.1462-2920.2004.00589.x
29. Rubin HE, Alexander M (1983) Effect of nutrients on the rates of mineralisation of trace concentrations of phenol and p-nitrophenol. Environ Sci Technol 17:104-107. doi: 10.1021/es00108a008
30. Schmidt SK, Alexander M (1985) Effects of dissolved organic carbon and second substrates on the biodegradation of organic compounds at low concentrations. Appl Environ Microbiol 49:822-827
31. Schwarzenbach R, Escher BI, Fenner K, Hofstetter TB, Johnson CA, von Gunten U, Wehrli B (2006) The challenge of micropollutants in aquatic systems. Science 313:1072-1077. doi: 10.1126/science.1127291
32. Smith KEC, Thullner M, Wick LY, Harms H (2009) Sorption to humic acids enhances polycyclic aromatic hydrocarbon biodegradation. Environ Sci Technol 43:7205-7211. doi: 10.1021/es803661s
33. Sniegowski K, Bers K, Van Goetem K, Ryckeboer J, Jaeken P, Spanoghe P, Springael D (2011) Improvement of pesticide mineralization in on-farm biopurification systems by bioaugmentation with pesticide-primed soil. FEMS Microbiol Ecol 76:64-73. doi: 10.1111/j.1574-6941.2010.01031.x
34. Sørensen SR, Simonsen A, Aamand J (2009) Constitutive mineralization of low concentrations of the herbicide linuron by a Variovorax sp. strain. FEMS Microbiol Lett 292:291-296. doi: 10.1111/j.1574-6968.2009. 01501.x
35. Sørensen SR, Holtze MS, Simonsen A, Aamand J (2007) Degradation and mineralization of nanomolar concentrations of the herbicide dichlobenil and its persistent metabolite 2,6-dichlorobenzamide by Aminobacter spp. isolated from dichlobenil-treated soils. Appl Environ Microbiol 73:399-406. doi: 10.1128/aem.01498-06
36. Sørensen SR, Bending GD, Jacobsen CS, Walker A, Aamand J (2003) Microbial degradation of isoproturon and related phenylurea herbicides in and below agricultural fields. FEMS Microbiol Ecol 45:1-11. doi: 10.1016/S0168-6496(03)00127-2
37. Toräng L, Nyholm N, Albrechtsen H-J (2003) Shifts in biodegradation kinetics of the herbicides MCPP and 2,4-D at low concentrations in aerobic aquifer materials. Environ Sci Technol 37:3095-3103. doi: 10.1021/es026307a
38. van der Meer JR, Roelofsen W, Schraa G, Zehnder AJB (1987) Degradation of low concentrations of dichlorobenzenes and 1,2,4-trichlorobenzene by Pseudomonas sp. strain P51 in nonsterile soil columns. FEMS Microbiol Lett 45:333-341. doi: 10.1111/j.1574-6968.1987.tb02410.x
39. Van Moorleghem C, Six L, Degryse F, Smolders E, Merckx R (2011) Effect of organic P forms and P present in inorganic colloids on the determination of dissolved P in environmental samples by the diffusive gradient in thin films technique, ion chromatography, and colorimetry. Anal Chem 83:5317-5323. doi: 10.1021/ac200748e
40. Wick LY, Pasche N, Bernasconi SM, Pelz O, Harms H (2003) Characterization of multiple-substrate utilization by anthracene-degrading Mycobacterium frederiksbergense LB501T. Appl Environ Microbiol 69:6133-6142. doi: 10.1128/AEM.69.10.6133-6142.2003
41. Wiggins BA, Alexander M (1988) Role of chemical concentration and second carbon sources in acclimation of microbial communities for biodegradation. Appl Environ Microbiol 54:2803-2807