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Effect of the anti-inflammatory drug diclofenac on lipid composition of bacterial strain Raoultella sp. KDF8

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Abstract

The strain Raoultella sp. KDF8 was cultivated on three sources of carbon and energy, glycerol, ethanol and diclofenac, for periods of time ranging from 24 to 72 h. Using thin-layer chromatography, nine classes of phospholipids were detected and the amount of phosphatidylethanolamine (PtdEtn) decreased with increasing cultivation time. Conversely, the ratio of phospholipids having three or four acyls (acyl-phosphatidylglycerol (APtdGro), N-acyl-PtdEtn (NAPtdEtn) and cardiolipin (Ptd2Gro) increased during cultivation. GC-MS analysis showed that the percentage of fatty acids containing a cyclopropane ring increased almost tenfold whereas the amount of fatty acids bearing even-numbered chains dropped to less than one-third after 24 h and 72 h in cultures on glycerol and diclofenac, respectively. Shotgun analysis showed significant changes in the representation of molecular species of phospholipids. For instance, there was a 36-fold change in the ratio of 16:1/16:1/16:1-APtdGro to c17:0/c17:0/c17:0-APtdGro and a 12-fold ratio change for 16:1/16:1/16:1-NAPtdEtn to c17:0/c17:0/c17:0-NAPtdEtn; the Ptd2Gro ratio of 16:1 to c17:0 acids equalled 1750. Our results show that the bacteria overcome destabilization of the inner cytoplasmic cell membrane and a bacterial outer membrane by altering the geometric arrangement of acyl chains, i.e. switching from monounsaturated to cyclopropane fatty acids (16:1 versus c17:0).

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References

  • Aluyi HS, Boote V, Drucker DB, Wilson JM, Ling YH (1992) Analysis of polar lipids from some representative enterobacteria, Plesiomonas and Acinetobacter by fast atom bombardment-mass spectrometry. J Appl Microbiol 73:426–432

    CAS  Google Scholar 

  • Bernat P, Siewiera P, Sobon A, Długonski J (2014) Phospholipids and protein adaptation of Pseudomonas sp. to the xenoestrogen tributyltin chloride (TBT). World J Microbiol Biotechnol 30:2343–2350

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Google Scholar 

  • Broniatowski M, Mastalerz P, Flasiński M (2015) Studies of the interactions of ursane-type bioactive terpenes with the model of Escherichia coli inner membrane-Langmuir monolayer approach. Biochim Biophys Acta 1848:469–476

    CAS  PubMed  Google Scholar 

  • Broniatowski M, Sobolewska K, Flasiński M, Wydro P (2016) Studies on the interactions of bisphenols with anionic phospholipids of decomposer membranes in model systems. Biochim Biophys Acta 1858:756–766

    CAS  PubMed  Google Scholar 

  • Caracciolo AB, Topp E, Grenni P (2015) Pharmaceuticals in the environment: biodegradation and effects on natural microbial communities. A review. J Pharm Biomed Anal 106:25–36

    Google Scholar 

  • Cryer B, Feldman M (1998) Cyclooxygenase-2 selectivity of widely used nonsteroidal anti-inflammatory drugs. Am J Med 104:413–421

    CAS  PubMed  Google Scholar 

  • Dembitsky VM, Rezanka T, Bychek IA (1992) Fatty-acids and phospholipids from lichens of the order Lecanorales. Phytochemistry 31:851–853

    Google Scholar 

  • Domaradzka D, Guzik U, Hupert-Kocurek K, Wojcieszynska D (2016) Toxicity of diclofenac and its biotransformation by Raoultella sp. DD4. Pol J Environ Stud 25:2211–2216

    CAS  Google Scholar 

  • Drancourt M, Bollet C, Carta A, Rousselier P (2001) Phylogenetic analyses of Klebsiella species delineate Klebsiella and Raoultella gen. nov., with description of Raoultella ornithinolytica comb, nov., Raoultella terrigena comb. nov and Raoultella planticola comb. nov. Int J Syst Evol Microbiol 51:925–932

    CAS  PubMed  Google Scholar 

  • Duldhardt J, Gaebel L, Chrzanowski L, Nijenhuis I, Hartig C, Schauer F, Heipieper HJ (2010) Adaptation of anaerobically grown Thauera aromatica, Geobacter sulfurreducens and Desulfococcus multivorans to organic solvents on the level of membrane fatty acid composition. Microb Biotechnol 3:201–209

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dutta NK, Mazumdar K, Dastidar SG, Park JH (2007) Activity of diclofenac used alone and in combination with streptomycin against Mycobacterium tuberculosis in mice. Int J Antimicrob Agents 30:336–340

    CAS  PubMed  Google Scholar 

  • Ferreira JV, Capello TM, Siqueira LJ, Lago JH, Caseli L (2016) Mechanism of action of thymol on cell membranes investigated through lipid Langmuir monolayers at the air-water interface and molecular simulation. Langmuir 32:3234–3241

    CAS  PubMed  Google Scholar 

  • Han X, Gross RW (2003) Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry: a bridge to lipidomics. J Lipid Res 44:1071–1079

    CAS  PubMed  Google Scholar 

  • Heipieper HJ, Meinhardt F, Segura A (2003) The cis-trans isomerase of unsaturated fatty acids in Pseudomonas and Vibrio: biochemistry, molecular biology and physiological function of a unique stress adaptive mechanism. FEMS Microbiol Lett 229:1–7

    CAS  PubMed  Google Scholar 

  • Holmback J, Karlsson AA, Arnoldsson KC (2001) Characterization of N-acylphosphatidylethanolamine and acylphosphatidylglycerol in oats. Lipids 36:153–165

    CAS  PubMed  Google Scholar 

  • Hsu FF, Turk J (2005) Electrospray ionization with low-energy collisionally activated dissociation tandem mass spectrometry of complex lipids: structural characterization and mechanisms of fragmentation. In: Byrdwell WC (ed) Modern methods for lipid analysis by liquid chromatography. AOCS Publishing, Urbana, pp 61–178

    Google Scholar 

  • Hsu FF, Turk J (2009) Electrospray ionization with low-energy collisionally activated dissociation tandem mass spectrometry of glycerophospholipids: mechanisms of fragmentation and structural characterization. J Chromatogr B Anal Technol Biomed Life Sci 877:2673–2695

    CAS  Google Scholar 

  • Hsu FF, Turk J, Shi Y, Groisman EA (2004) Characterization of acylphosphatidylglycerols from Salmonella typhimurium by tandem mass spectrometry with electrospray ionization. J Am Soc Mass Spectrom 15:1–11

    CAS  PubMed  Google Scholar 

  • Ingram LO (1977) Preferential inhibition of phosphatidyl ethanolamine synthesis in E. coli by alcohols. Can J Microbiol 23:779–789

    CAS  PubMed  Google Scholar 

  • Ingram LO, Ley KD, Hoffmann EM (1978) Drug-induced changes in lipid composition of E. coli and of mammalian cells in culture: ethanol, pentobarbital, and chlorpromazine. Life Sci 22:489–494

    CAS  PubMed  Google Scholar 

  • Jasim R, Han ML, Zhu Y, Hu X, Hussein MH, Lin YW, Zhou QT, Dong CYD, Li J, Velkov T (2018) Lipidomic analysis of the outer membrane vesicles from paired polymyxin-susceptible and -resistant Klebsiella pneumonia clinical isolates. Int J Mol Sci 19:2356

    PubMed Central  Google Scholar 

  • Knittelfelder OL, Weberhofer BP, Eichmann TO, Kohlwein SD, Rechberger GN (2014) A versatile ultra-high performance LC-MS method for lipid profiling. J Chromatogr B Anal Technol Biomed Life Sci 951–952:119–128

    Google Scholar 

  • Luo Y, Javed MA, Deneer H, Chen X (2018) Nutrient depletion-induced production of tri-acylated glycerophospholipids in Acinetobacter radioresistens. Sci Rep 8:7470

    PubMed  PubMed Central  Google Scholar 

  • Meerburg F, Hennebel T, Vanhaecke L, Verstraete W, Boon N (2012) Diclofenac and 2-anilinophenylacetate degradation by combined activity of biogenic manganese oxides and silver. Microb Biotechnol 5:388–395

    PubMed  PubMed Central  Google Scholar 

  • Moreira IS, Bessa VS, Murgolo S, Piccirillo C, Mascolo G, Castro PML (2018) Biodegradation of diclofenac by the bacterial strain Labrys portucalensis F11. Ecotoxicol Environ Saf 152:104–113

    CAS  PubMed  Google Scholar 

  • Novak J, Sokolova L, Lemr K, Pluhacek T, Palyzova A, Havlicek V (2017) Batch-processing of imaging or liquid-chromatography mass spectrometry datasets and de novo sequencing of polyketide siderophores. Biochim Biophys Acta 1865:768–775

    CAS  Google Scholar 

  • Palyzová A, Zahradník J, Marešová H, Sokolová L, Kyslíková E, Grulich M, Štěpánek V, Řezanka T, Kyslík P (2018) Potential of the strain Raoultella sp. KDF8 for removal of analgesics. Folia Microbiol 63:273–282

    Google Scholar 

  • Palyzová A, Marešová H, Zahradník J, Řezanka T (2019) Characterization of the catabolic pathway of diclofenac in Raoultella sp. KDF8. Int Biodeterior Biodegradation 137:88–94

    Google Scholar 

  • Perly B, Smith ICP, Jarrell HC (1985) Effects of the replacement of a double bond by a cyclopropane ring in phosphatidylethanolamines: a 2H NMR study of phase transitions and molecular organization. Biochemistry 24:1055–1063

    CAS  PubMed  Google Scholar 

  • Poger D, Mark AE (2015) A ring to rule them all: the effect of cyclopropane fatty acids on the fluidity of lipid bilayers. J Phys Chem B 119:5487–5495

    CAS  PubMed  Google Scholar 

  • Radjenovic J, Petrovic M, Barcelo D (2009) Fate and distribution of pharmaceuticals in wastewater and sewage sludge of the conventional activated sludge (CAS) and advanced membrane bioreactor (MBR) treatment. Water Res 43:831–841

    CAS  PubMed  Google Scholar 

  • Sánchez M, Garbi C, Martínez-Álvarez R, Ortiz LT, Allende JL, Martín M (2005) Klebsiella planticola strain DSZ mineralizes simazine: physiological adaptations involved in the process. Appl Microbiol Biotechnol 66:589–596

    PubMed  Google Scholar 

  • Santos IC, Smuts J, Choi WS, Kim Y, Kim SB, Schug KA (2018) Analysis of bacterial FAMEs using gas chromatography-vacuum ultraviolet spectroscopy for the identification and discrimination of bacteria. Talanta 182:536–543

    CAS  PubMed  Google Scholar 

  • Segura A, Duque E, Mosqueda G, Ramos JL, Junker F (1999) Multiple responses of Gram-negative bacteria to organic solvents. Environ Microbiol 1:191–198

    CAS  PubMed  Google Scholar 

  • Shabala L, Ross T (2008) Cyclopropane fatty acids improve Escherichia coli survival in acidified minimal media by reducing membrane permeability to H+ and enhanced ability to extrude H+. Res Microbiol 159:458–461

    CAS  PubMed  Google Scholar 

  • Sohlenkamp C, Geiger O (2016) Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev 40:133–159

    CAS  PubMed  Google Scholar 

  • Suklabaidya S, Debnath P, Dey B, Bhattacharjee D, Hussain SA (2018) Interaction of an antibiotic—norfloxacin with lipid membrane. Mater Today Proc 5:2373–2380

    CAS  Google Scholar 

  • Vancura A, Rezanka T, Marsálek J, Melzoch K, Basarova G, Kristan V (1988) Metabolism of L-threonine and fatty-acids and tylosin biosynthesis in Streptomyces fradiae. FEMS Microbiol Lett 49:411–415

    CAS  Google Scholar 

  • Wardhan R, Mudgal P (2017) Textbook of membrane biology. Springer Nature, London

    Google Scholar 

  • Wojcik A, Pawlowski M, Wydro P, Broniatowski M (2018) Effects of polychlorinated pesticides and their metabolites on phospholipid organization in model microbial membranes. J Phys Chem B 122:12017–12030

    CAS  PubMed  Google Scholar 

  • Yagüe G, Segovia M, Valero Guillén PL (2006) Acyl phosphatidylglycerol: a major phospholipid of Corynebacterium amycolatum. FEMS Microbiol Lett 151:125–130

    Google Scholar 

Download references

Acknowledgments

This research was supported by the Ministry of Education, Youth and Sports of the Czech Republic (LO1509) and the Epsilon programme of the Technology Agency of the Czech Republic (TH02030337).

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Correspondence to Tomáš Řezanka.

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Palyzová, A., Marešová, H., Novák, J. et al. Effect of the anti-inflammatory drug diclofenac on lipid composition of bacterial strain Raoultella sp. KDF8. Folia Microbiol 65, 763–773 (2020). https://doi.org/10.1007/s12223-020-00790-9

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