Abstract
A bacterial strain capable of aerobic degradation of 4-fluorocinnamic acid (4-FCA) as the sole source of carbon and energy was isolated from a biofilm reactor operating for the treatment of 2-fluorophenol. The organism, designated as strain S2, was identified by 16S rRNA gene analysis as a member of the genus Rhodococcus. Strain S2 was able to mineralize 4-FCA as sole carbon and energy source. In the presence of a conventional carbon source (sodium acetate [SA]), growth rate of strain S2 was enhanced from 0.04 to 0.14 h−1 when the culture medium was fed with 0.5 mM of 4-FCA, and the time for complete removal of 4-FCA decreased from 216 to 50 h. When grown in SA-supplemented medium, 4-FCA concentrations up to 1 mM did not affect the length of the lag phase, and for 4-FCA concentrations up to 3 mM, strain S2 was able to completely remove the target fluorinated compound. 4-Fluorobenzoate (4-FBA) was transiently formed in the culture medium, reaching concentrations up to 1.7 mM when the cultures were supplemented with 3.5 mM of 4-FCA. Trans,trans-muconate was also transiently formed as a metabolic intermediate. Compounds with molecular mass compatible with 3-carboxymuconate and 3-oxoadipate were also detected in the culture medium. Strain S2 was able to mineralize a range of other haloorganic compounds, including 2-fluorophenol, to which the biofilm reactor had been exposed. To our knowledge, this is the first time that mineralization of 4-FCA as the sole carbon source by a single bacterial culture is reported.
Similar content being viewed by others
References
Amorim CL, Carvalho MF, Afonso CMM, Castro PML (2013) Biodegradation of fluoroanilines by the wild strain Labrys portucalensis. Int Biodeterior Biodegrad 80:10–15. doi:10.1016/j.ibiod.2013.02.001
Boersma MG, Solyanikova IP, Van Berkel WJ, Vervoort J, Golovleva LA, Rietjens IM (2001) 19F NMR metabolomics for the elucidation of microbial degradation pathways of fluorophenols. J Ind Microbiol Biotechnol 26:22–34. doi:10.1038/sj.jim.7000027
Boersma FGH, McRoberts WC, Cobb SL, Murphy CD (2004) A 19F NMR study of fluorobenzoate biodegradation by Sphingomonas sp. HB-1. FEMS Microbiol Lett 237:355–361. doi:10.1016/j.femsle.2004.06.052
Briglia M, Rainey FA, Stackebrandt E, Schraa G, Salkinoja-Salonen MS (1996) Rhodococcus percolatus sp. nov., a bacterium degrading 2,4,6-trichlorophenol. Int J Syst Bacteriol 46:23–30. doi:10.1099/00207713-46-1-23
Cao B, Karthiga N, Loh KC (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol 85:207–228. doi:10.1007/s00253-009-2192-4
Carvalho MF, Ferreira Jorge R, Pacheco CC, De Marco P, Castro PML (2005) Isolation and properties of a pure bacterial strain capable of fluorobenzene degradation as sole carbon and energy source. Environ Microbiol 7:294–298. doi:10.1111/j.1462-2920.2004.00714.x
Creaser C, Freitas dos Santos LF, Lamarca DG, New A, Wolff JC (2002) Biodegradation studies of 4-fluorobenzoic acid and 4-fluorocinnamic acid: an evaluation of membrane inlet mass spectrometry as an alternative to high performance liquid chromatography and ion chromatography. Anal Chim Acta 454:137–145. doi:10.1016/S0003-2670(01)01514-8
Duque AF, Bessa VS, Carvalho MF, Castro PML (2011) Bioaugmentation of a rotating biological contactor for degradation of 2-fluorophenol. Bioresour Technol 102:9300–9303. doi:10.1016/j.biortech.2011.07.003
Duque AF, Hasan S a, Bessa VS, Carvalho MF, Samin G, Janssen DB, Castro PML (2012) Isolation and characterization of a Rhodococcus strain able to degrade 2-fluorophenol. Appl Microbiol Biotechnol 95:511–520. doi:10.1007/s00253-011-3696-2
Ferreira MIM, Marchesi JR, Janssen DB (2008) Degradation of 4-fluorophenol by Arthrobacter sp. strain IF1. Appl Microbiol Biotechnol 78:709–717. doi:10.1007/s00253-008-1343-3
Freitas dos Santos LMF, Spicq A, New AP, Lo Biundo G, Wolff JC, Edwards A (2001) Aerobic biotransformation of 4-fluorocinnamic acid to 4-fluorobenzoic acid. Biodegrad 12:23–29. doi:10.1023/A:1011973824171
Gerus I, Glushchenko A, Kurioz Y, Reznikov Y, Tereshchenko O (2004) Sticking of liquid crystal on photosensitive polymer layers. Opto-Electron Rev 12:281–284. doi:10.1117/12.714853
Ghosh A, Paul D, Prakash D, Mayilraj S, Jain RK (2006) Rhodococcus imtechensis sp. nov., a nitrophenol-degrading actinomycete. Int J Syst Evol Microbiol 56:1965–1969. doi:10.1099/ijs.0.63939-0
Hasan SA, Ferreira MIM, Koetsier MJ, Arif MI, Janssen DB (2011) Complete biodegradation of 4-fluorocinnamic acid by a consortium comprising Arthrobacter sp. Strain G1 and Ralstonia sp. strain H1. Appl Environ Microbiol 77:572–579. doi:10.1128/AEM.00393-10
Hasan SA, Wietzes P, Janssen DB (2012) Biodegradation kinetics of 4-fluorocinnamic acid by a consortium of Arthrobacter and Ralstonia strains. Biodegrad 23:117–125. doi:10.1007/s10532-011-9491-z
Iwasaki I, Utsumi S, Hagino K, Ozawa T (1956) A new spectrophotometric method for the determination of small amounts of chloride using the mercury thiocyanate method. J Chem Soc Japan 29:860–864. doi:10.1246/bcsj.29.860
Janssen DB, Dinkla IJT, Poelarends GJ, Terpstra P (2005) Bacterial degradation of xenobiotic compounds: evolution and distribution of novel enzyme activities. Environ Microbiol 7:1868–1882. doi:10.1111/j.1462-2920.2005.00966.x
Juang RS, Tsai SY (2006) Growth kinetics of Pseudomonas putida in the biodegradation of single and mixed phenol and sodium salicylate. Biochem Eng J 31:133–140. doi:10.1016/j.bej.2006.05.025
Key BD, Howell RD, Criddle CS (1997) Fluorinated organics in the biosphere. Environ Sci Technol 31:2445–2454. doi:10.1021/es961007c
Kwon KH, Yeom SH (2009) Optimal microbial adaptation routes for the rapid degradation of high concentration of phenol. Bioproc Biosyst Eng 32:435–442. doi:10.1007/s00449-008-0263-z
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175
Larkin MJ, Kulakov LA, Allen CCR (2005) Biodegradation and Rhodococcus – masters of catabolic versatility. Curr Opin Biotechnol 16:282–290. doi:10.1016/j.copbio.2005.04.007
Loh KC, Yu YG (2000) Kinetics of carbazole degradation by Pseudomonas putida in presence of sodium salicylate. Water Res 34:4131–4138. doi:10.1016/S0043-1354(00)00174-3
Mamma D, Kalogeris E, Papadopoulos N, Hatzinikolaou DG, Christrakopoulos P, Kekos D (2004) Biodegradation of phenol by acclimatized Pseudomonas putida cells using glucose as an added growth substrate. J Environ Sci Health, Part A-Toxic/Hazard Subst Environ Eng 39:2093–2104. doi:10.1081/ESE-120039377
Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35:162–177. doi:10.1016/j.envint.2008.07.018
Moreira IS, Amorim CL, Carvalho MF, Castro PML (2012a) Co-metabolic degradation of chlorobenzene by the fluorobenzene degrading wild strain Labrys portucalensis. Int Biodeterior Biodegrad 72:76–81. doi:10.1016/j.ibiod.2012.05.013
Moreira IS, Amorim CL, Carvalho MF, Castro PML (2012b) Degradation of difluorobenzenes by the wild strain Labrys portucalensis. Biodegrad 23:653–662. doi:10.1007/s10532-012-9541-1
Murphy CD, Clark BR, Amadio J (2009) Metabolism of fluoroorganic compounds in microorganisms: impacts for the environment and the production of fine Chemicals. Appl Microbiol Biotechnol 84:617–629. doi:10.1007/s00253-009-2127-0
Natarajan R, Azerad R, Badet B, Copin E (2005) Microbial cleavage of C–F bond. J Fluor Chem 126:425–436. doi:10.1016/j.jfluchem.2004.12.001
New AP, Freitas dos Santos LM, Lo Biundo G, Spicq A (2000) Analytical techniques used for monitoring the biodegradation of fluorinated compounds in waste streams from pharmaceutical production. J Chromatogr A 889:177–184. doi:10.1016/S0021-9673(00)00571-9
Oltmanns RH, Müller R, Otto MK, Lingens F (1989) Evidence for a new pathway in the bacterial degradation of 4-fluorobenzoate. Appl Environ Microbiol 55:2499–2504
Osuna MB, Sipma J, Emanuelsson ME, Carvalho MF, Castro PML (2008) Biodegradation of 2-fluorobenzoate and dichloromethane under simultaneous and sequential alternating pollutant feeding. Water Res 42:3857–3869. doi:10.1016/j.watres.2008.05.011
Schlömann M, Fischer P, Schmidt E, Knackmuss HJ (1990) Enzymatic formation, stability, and spontaneous reactions of 4-fluoromuconolactone, a metabolite of the bacterial degradation of 4-fluorobenzoate. J Bacteriol 172:5119–5129
Schreiber A, Hellwig M, Dorn E, Reineke W, Knackmuss HJ (1980) Critical reactions in fluorobenzoic acid degradation. Appl Environ Microbiol 39:58–67
Stanier RY, Ingraham JL (1954) Protocatechuic acid oxidase. J Biol Chem 210:799–808
Strunk N, Engesser KH (2012) Degradation of fluorobenzene and its central metabolites 3-fluorocatechol and 2-fluoromuconate by Burkholderia fungorum FLU100. Appl Microbiol Biotechnol 97:5605–5614. doi:10.1007/s00253-012-4388-2
Sun FM, Wang JS, Traxler RW (2000) A novel ortho-dehalogenation reaction of 2-chlorocinnamic acid catalyzed by the pink yeast Rhodotorula rubra Y-1529. Chemosphere 40:1417–1425. doi:10.1016/S0045-6535(99)00316-1
Wang SJ, Loh KC (2001) Biotransformation kinetics of Pseudomonas putida for cometabolism of phenol and 4-chlorophenol in the presence of sodium glutamate. Biodegrad 12:189–199. doi:10.1023/A:1013170322269
Wang Z, Xu J, Li Y, Wang K, Wang Y, Hong Q, Li W, Li S (2010) Rhodococcus jialingiae sp. nov., an actinobacterium isolated from sludge of a carbendazim wastewater treatment facility. Int J Syst Evol Microbiol 60:378–381. doi:10.1099/ijs.0.013219-0
Xu JL, He J, Wang ZC, Wang K, Li WJ, Tang SK, Li SP (2007) Rhodococcus qingshengii sp. nov., a carbendazim-degrading bacterium. Int J Syst Evol Microbiol 57:2754–2757. doi:10.1099/ijs.0.55095-0
Yoon JH, Cho YG, Kang SS, Kim SB, Lee ST, Park YH (2000) Rhodococcus koreensis sp. nov., a 2,4-dinitrophenol-degrading bacterium. Int J Syst Evol Microbiol 50:1193–1201. doi:10.1099/00207713-50-3-1193
Yu YG, Loh KC (2002) Inhibition of p-cresol on aerobic biodegradation of carbazole and sodium salicylate by Pseudomonas putida. Water Res 36:1794–1802. doi:10.1016/S0043-1354(01)00387-6
Acknowledgments
We thank Prof. Dick B. Janssen for helpful discussions and for revising the manuscript. C.L. Amorim and M.F. Carvalho wish to acknowledge a research grant from Fundação para a Ciência e Tecnologia (FCT), Portugal (Ref. SFRH/BD/47109/2008 and SFRH/BPD/44670/2008, respectively) and Fundo Social Europeu (Programa Operacional Potencial Humano (POPH), Quadro de Referência Estratégico Nacional (QREN))). This work was supported by FCT through the projects PTDC/BIO/67306/2006, PTDC/EBB-EBI/111699/2009 and PEst-OE/EQB/LA0016/2011.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Amorim, C.L., Ferreira, A.C.S., Carvalho, M.F. et al. Mineralization of 4-fluorocinnamic acid by a Rhodococcus strain. Appl Microbiol Biotechnol 98, 1893–1905 (2014). https://doi.org/10.1007/s00253-013-5149-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-013-5149-6