Biodegradation of pentafluorosulfanyl-substituted aminophenol in Pseudomonas spp.

  • Marta Saccomanno
  • Sabir Hussain
  • Neil K. O’Connor
  • Petr Beier
  • Mate Somlyay
  • Robert Konrat
  • Cormac D. Murphy
Original Paper
First Online:
Received:
Accepted:

Abstract

The pentafluorosulfanyl (SF5–) substituent conveys properties that are beneficial to drugs and agrochemicals. As synthetic methodologies improve the number of compounds containing this group will expand and these chemicals may be viewed as emerging pollutants. As many microorganisms can degrade aromatic xenobiotics, we investigated the catabolism of SF5-substituted aminophenols by bacteria and found that some Pseudomonas spp. can utilise these compounds as sole carbon and energy sources. GC–MS analysis of the culture supernatants from cultures grown in 5-(pentafluorosulfanyl) 2-aminophenol demonstrated the presence of the N-acetylated derivative of the starting substrate and 4-(pentafluorosulfanyl)catechol. Biotransformation experiments with re-suspended cells were also conducted and fluorine-19 NMR analyses of the organic extract and aqueous fraction from suspended cell experiments revealed new resonances of SF5-substituted intermediates. Supplementation of suspended cell cultures with yeast extract dramatically improved the degradation of the substrate as well as the release of fluoride ion. 4-(Pentafluorosulfanyl)catechol was shown to be a shunt metabolite and toxic to some of the bacteria. This is the first study to demonstrate that microorganisms can biodegrade SF5-substituted aromatic compounds releasing fluoride ion, and biotransform them generating a toxic metabolite.

Keywords

Biodegradation Emerging pollutant Fluoride Pentafluorosulfanyl Pseudomonas 
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Notes

Acknowledgements

This work was supported by the Initial Training Network, FLUOR21, funded by the FP7 Marie Curie Actions of the European Commission (FP7-PEOPLE-2013-ITN-607787). SH was supported by an Irish Research Council Government of Ireland Postdoctoral Fellowship.

Supplementary material

10532_2018_9827_MOESM1_ESM.docx (147 kb)
Supplementary material 1 (DOCX 146 kb)

References

  1. Altomonte S, Zanda M (2012) Synthetic chemistry and biological activity of pentafluorosulphanyl (SF5) organic molecules. J Fluorine Chem 143:57–93.  https://doi.org/10.1016/j.jfluchem.2012.06.030 CrossRefGoogle Scholar
  2. Arora PK, Srivastava A, Singh VP (2014) Novel degradation pathway of 4-chloro-2-aminophenol via 4-chlorocatechol in Burkholderia sp. RKJ 800. Environ Sci Pollut Res 21(3):2298–2304.  https://doi.org/10.1007/s11356-013-2167-y CrossRefGoogle Scholar
  3. Beier P, Pastyrikova T (2011) Hydroxylation of nitro-(pentafluorosulfanyl)benzenes via vicarious nucleophilic substitution of hydrogen. Tetrahedron Lett 52(34):4392–4394.  https://doi.org/10.1016/j.tetlet.2011.06.011 CrossRefGoogle Scholar
  4. Davis KJ, He Z, Somerville CC, Spain CJ (1999) Genetic and biochemical comparison of 2-aminophenol 1,6-dioxygenase of Pseudomonas pseudoalcaligenes JS45 to meta-cleavage dioxygenases: divergent evolution of 2-aminophenol meta-cleavage pathway. Arch Microbiol 172(5):330–339.  https://doi.org/10.1007/s002030050787 CrossRefPubMedGoogle Scholar
  5. Diaz E, Jimenez JI, Nogales J (2013) Aerobic degradation of aromatic compounds. Curr Opin Biotechnol 24:431–442.  https://doi.org/10.1016/j.copbio.2012.10.010 CrossRefPubMedGoogle Scholar
  6. Gaillard M, Vallaeys T, Vorholter FJ, Minoia M, Werlen C, Sentchilo V, Puhler A, van der Meer JR (2006) The clc element of Pseudomonas sp strain B13, a genomic island with various catabolic properties. J Bacteriol 188(5):1999–2013.  https://doi.org/10.1128/jb.188.5.1999-2013.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Gillis EP, Eastman KJ, Hill MD, Donnelly DJ, Meanwell NA (2015) Applications of fluorine in medicinal chemistry. J Med Chem 58(21):8315–8359.  https://doi.org/10.1021/acs.jmedchem.5b00258 CrossRefPubMedGoogle Scholar
  8. Hendriks CMM, Penning TM, Zang TZ, Wiemuth D, Grunder S, Sanhueza IA, Schoenebeck F, Bolm C (2015) Pentafluorosulfanyl-containing flufenamic acid analogs: syntheses, properties and biological activities. Bioorg Med Chem Lett 25(20):4437–4440.  https://doi.org/10.1016/j.bmcl.2015.09.012 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Hughes D, Clark BR, Murphy CD (2011) Biodegradation of polyfluorinated biphenyl in bacteria. Biodegradation 22:741–749.  https://doi.org/10.1007/s10532-010-9411-7 CrossRefPubMedGoogle Scholar
  10. Jackson DA, Mabury SA (2009) Environmental properties of pentafluorosulfanyl compounds: physical properties and photodegradation. Environ Toxicol Chem 28(9):1866–1873CrossRefPubMedGoogle Scholar
  11. Jeschke P (2010) The unique role of halogen substituents in the design of modern agrochemicals. Pest Manag Sci 66(1):10–27.  https://doi.org/10.1002/ps.1829 CrossRefPubMedGoogle Scholar
  12. Kavanagh E, Winn M, Gabhann CN, O’Connor NK, Beier P, Murphy CD (2014) Microbial biotransformation of aryl sulfanylpentafluorides. Environ Sci Pollut Res 21(1):753–758.  https://doi.org/10.1007/s11356-013-1985-2 CrossRefGoogle Scholar
  13. Kiel M, Engesser KH (2015) The biodegradation vs. biotransformation of fluorosubstituted aromatics. Appl Microbiol Biotechnol 99(18):7433–7464.  https://doi.org/10.1007/s00253-015-6817-5 CrossRefPubMedGoogle Scholar
  14. Lim DS, Choi JS, Pak CS, Welch JT (2007) Synthesis and herbicidal activity of a pentafluorosulfanyl analog of trifluralin. J Pestic Sci 32(3):255–259.  https://doi.org/10.1584/jpestics.G06-50 CrossRefGoogle Scholar
  15. Murphy CD (2007) The application of F-19 nuclear magnetic resonance to investigate microbial biotransformations of organofluorine compounds. OMICS 11(3):314–324.  https://doi.org/10.1089/omi.2007.0002 CrossRefPubMedGoogle Scholar
  16. Murphy CD (2010) Biodegradation and biotransformation of organofluorine compounds. Biotechnol Lett 32(3):351–359.  https://doi.org/10.1007/s10529-009-0174-3 CrossRefPubMedGoogle Scholar
  17. Murphy CD, Sandford G (2015) Recent advances in fluorination techniques and their anticipated impact on drug metabolism and toxicity. Expert Opin Drug Metab Toxicol 11(4):589–599.  https://doi.org/10.1517/17425255.2015.1020295 CrossRefPubMedGoogle Scholar
  18. Savoie PR, Welch JT (2015) Preparation and utility of organic pentafluorosulfanyl-containing compounds. Chem Rev 115(2):1130–1190.  https://doi.org/10.1021/cr500336u CrossRefPubMedGoogle Scholar
  19. Takenaka S, Murakami S, Shinke R, Aoki K (1998) Metabolism of 2-aminophenol by Pseudomonas sp. AP-3: modified meta-cleavage pathway. Arch Microbiol 170(2):132–137.  https://doi.org/10.1007/s002030050624 CrossRefPubMedGoogle Scholar
  20. Takenaka S, Murakami S, Kim YJ, Aoki K (2000) Complete nucleotide sequence and functional analysis of the genes for 2-aminophenol metabolism from Pseudomonas sp AP-3. Arch Microbiol 174(4):265–272.  https://doi.org/10.1007/s002030000203 CrossRefPubMedGoogle Scholar
  21. Vida N, Pastyrikova T, Klepetarova B, Beier P (2014) Synthesis of aliphatic sulfur pentafluorides by oxidation of SF5-containing anisole, phenols, and anilines. J Org Chem 79(18):8906–8911.  https://doi.org/10.1021/jo501562z CrossRefPubMedGoogle Scholar
  22. Vida N, Vaclavik J, Beier P (2016) Synthesis and reactivity of aliphatic sulfur pentafluorides from substituted (pentafluorosulfanyl)benzenes. Beilstein J Org Chem 12:110–116.  https://doi.org/10.3762/bjoc.12.12 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Welch JT, Lim DS (2007) The synthesis and biological activity of pentafluorosulfanyl analogs of fluoxetine, fenfluramine, and norfenfluramine. Bioorg Med Chem 15(21):6659–6666.  https://doi.org/10.1016/j.bmc.2007.08.012 CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.School of Biomolecular and Biomedical ScienceUniversity College DublinDublin 4Ireland
  2. 2.Institute of Organic Chemistry and BiochemistryAcademy of Sciences of the Czech RepublicPragueCzech Republic
  3. 3.Max F. Perutz LaboratoriesUniversity of ViennaViennaAustria
  4. 4.Dept of Environmental Science & EngineeringGovernment College UniversityFaisalabadPakistan

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