Environmentally Relevant Concentration of Bisphenol S Shows Slight Effects on SIHUMIx

. 2020 Sep 19 ; 8 (9) : . [epub] 20200919

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32961728
Odkazy

PubMed 32961728
PubMed Central PMC7564734
DOI 10.3390/microorganisms8091436
PII: microorganisms8091436
Knihovny.cz E-zdroje

Bisphenol S (BPS) is an industrial chemical used in the process of polymerization of polycarbonate plastics and epoxy resins and thus can be found in various plastic products and thermal papers. The microbiota disrupting effect of BPS on the community structure of the microbiome has already been reported, but little is known on how BPS affects bacterial activity and function. To analyze these effects, we cultivated the simplified human intestinal microbiota (SIHUMIx) in bioreactors at a concentration of 45 µM BPS. By determining biomass, growth of SIHUMIx was followed but no differences during BPS exposure were observed. To validate if the membrane composition was affected, fatty acid methyl esters (FAMEs) profiles were compared. Changes in the individual membrane fatty acid composition could not been described; however, the saturation level of the membranes slightly increased during BPS exposure. By applying targeted metabolomics to quantify short-chain fatty acids (SCFA), it was shown that the activity of SIHUMIx was unaffected. Metaproteomics revealed temporal effect on the community structure and function, showing that BPS has minor effects on the structure or functionality of SIHUMIx.

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Pjanic M. The role of polycarbonate monomer bisphenol-A in insulin resistance. PeerJ. 2017;5:e3809. doi: 10.7717/peerj.3809. PubMed DOI PMC

Arnold S.M., Clark K.E., Staples C.A., Klecka G.M., Dimond S.S., Caspers N., Hentges S.G. Relevance of drinking water as a source of human exposure to bisphenol A. J. Expo. Sci. Environ. Epidemiol. 2013;23:137–144. doi: 10.1038/jes.2012.66. PubMed DOI PMC

Rochester J.R., Bolden A.L. Bisphenol S and F: A Systematic Review and Comparison of the Hormonal Activity of Bisphenol A Substitutes. Environ. Health Perspect. 2015;123:643–650. doi: 10.1289/ehp.1408989. PubMed DOI PMC

Cano-Nicolau J., Vaillant C., Pellegrini E., Charlier T.D., Kah O., Coumailleau P. Estrogenic Effects of Several BPA Analogs in the Developing Zebrafish Brain. Front. Neurosci. 2016;10:112. doi: 10.3389/fnins.2016.00112. PubMed DOI PMC

ECHA . Inclusion of Substances of Very High Concern in the Candidate List for Eventual Inclusion in Annex XIV. Europeen Chemicals Agency; Helsinki, Finland: 2018.

Pal S., Sarkar K., Nath P.P., Mondal M., Khatun A., Paul G. Bisphenol S impairs blood functions and induces cardiovascular risks in rats. Toxicol. Rep. 2017;4:560–565. doi: 10.1016/j.toxrep.2017.10.006. PubMed DOI PMC

CHCC [(accessed on 5 December 2017)];Chemicals of High Concern to Children (CHCC) Reporting List. Available online: http://portal.mts-global.com/en/technical_update/CPIE-026-17.html.

Qiu W., Yang M., Liu S., Lei P., Hu L., Chen B., Wu M., Wang K.J. Toxic Effects of Bisphenol S Showing Immunomodulation in Fish Macrophages. Environ. Sci. Technol. 2018;52:831–838. doi: 10.1021/acs.est.7b04226. PubMed DOI

Tzatzarakis M.N., Vakonaki E., Kavvalakis M.P., Barmpas M., Kokkinakis E.N., Xenos K., Tsatsakis A.M. Biomonitoring of bisphenol A in hair of Greek population. Chemosphere. 2015;118:336–341. doi: 10.1016/j.chemosphere.2014.10.044. PubMed DOI

Gonzalez N., Cunha S.C., Monteiro C., Fernandes J.O., Marques M., Domingo J.L., Nadal M. Quantification of eight bisphenol analogues in blood and urine samples of workers in a hazardous waste incinerator. Environ. Res. 2019;176:108576. doi: 10.1016/j.envres.2019.108576. PubMed DOI

Jin H.B., Xie J.H., Mao L.L., Zhao M.R., Bai X.X., Wen J., Shen T., Wu P.F. Bisphenol analogue concentrations in human breast milk and their associations with postnatal infant growth. Environ. Pollut. 2020;259 doi: 10.1016/j.envpol.2019.113779. PubMed DOI

Liu M., Jia S., Dong T., Han Y., Xue J., Wanjaya E.R., Fang M. The occurrence of bisphenol plasticizers in paired dust and urine samples and its association with oxidative stress. Chemosphere. 2019;216:472–478. doi: 10.1016/j.chemosphere.2018.10.090. PubMed DOI

Kinross J.M., Darzi A.W., Nicholson J.K. Gut microbiome-host interactions in health and disease. Genome Med. 2011;3:14. doi: 10.1186/gm228. PubMed DOI PMC

Koppel N., Maini Rekdal V., Balskus E.P. Chemical transformation of xenobiotics by the human gut microbiota. Science. 2017;356 doi: 10.1126/science.aag2770. PubMed DOI PMC

Claus S.P., Guillou H., Ellero-Simatos S. The gut microbiota: A major player in the toxicity of environmental pollutants? NPJ Biofilms Microbiomes. 2016;2:16003. doi: 10.1038/npjbiofilms.2016.3. PubMed DOI PMC

Spanogiannopoulos P., Bess E.N., Carmody R.N., Turnbaugh P.J. The microbial pharmacists within us: A metagenomic view of xenobiotic metabolism. Nat. Rev. Microbiol. 2016;14:273–287. doi: 10.1038/nrmicro.2016.17. PubMed DOI PMC

Zhang W., Yin K., Chen L. Bacteria-mediated bisphenol A degradation. Appl. Microbiol. Biotechnol. 2013;97:5681–5689. doi: 10.1007/s00253-013-4949-z. PubMed DOI

Danzl E., Sei K., Soda S., Ike M., Fujita M. Biodegradation of bisphenol A, bisphenol F and bisphenol S in seawater. Int. J. Environ. Res. Public Health. 2009;6:1472–1484. doi: 10.3390/ijerph6041472. PubMed DOI PMC

Heipieper H.J., Weber F.J., Sikkema J., Keweloh H., de Bont J.A.M. Mechanisms of resistance of whole cells to toxic organic solvents. Trends Biotechnol. 1994;12:409–415. doi: 10.1016/0167-7799(94)90029-9. DOI

Hąc-Wydro K., Połeć K., Broniatowski M. The comparative analysis of the effect of environmental toxicants: Bisphenol A, S and F on model plant, fungi and bacteria membranes. The studies on multicomponent systems. J. Mol. Liq. 2019;289:111136. doi: 10.1016/j.molliq.2019.111136. DOI

Lai K.P., Chung Y.T., Li R., Wan H.T., Wong C.K. Bisphenol A alters gut microbiome: Comparative metagenomics analysis. Environ. Pollut. 2016;218:923–930. doi: 10.1016/j.envpol.2016.08.039. PubMed DOI

Catron T.R., Keely S.P., Brinkman N.E., Zurlinden T.J., Wood C.E., Wright J.R., Phelps D., Wheaton E., Kvasnicka A., Gaballah S., et al. Host Developmental Toxicity of BPA and BPA Alternatives Is Inversely Related to Microbiota Disruption in Zebrafish. Toxicol. Sci. 2019;167:468–483. doi: 10.1093/toxsci/kfy261. PubMed DOI

Krause J.L., Schaepe S.S., Fritz-Wallace K., Engelmann B., Rolle-Kampczyk U., Kleinsteuber S., Schattenberg F., Liu Z., Mueller S., Jehmlich N., et al. Following the community development of SIHUMIx—A new intestinal in vitro model for bioreactor use. Gut Microbes. 2019 doi: 10.1080/19490976.2019.1702431. PubMed DOI PMC

Schäpe S.S., Krause J.L., Engelmann B., Fritz-Wallace K., Schattenberg F., Liu Z., Müller S., Jehmlich N., Rolle-Kampczyk U., Herberth G., et al. The Simplified Human Intestinal Microbiota (SIHUMIx) Shows High Structural and Functional Resistance against Changing Transit Times in In Vitro Bioreactors. Microorganisms. 2019;7:641. doi: 10.3390/microorganisms7120641. PubMed DOI PMC

Becker N., Kunath J., Loh G., Blaut M. Human intestinal microbiota: Characterization of a simplified and stable gnotobiotic rat model. Gut Microbes. 2011;2:25–33. doi: 10.4161/gmic.2.1.14651. PubMed DOI

Wissenbach D.K., Oliphant K., Rolle-Kampczyk U., Yen S., Hoke H., Baumann S., Haange S.B., Verdu E.F., Allen-Vercoe E., von Bergen M. Optimization of metabolomics of defined in vitro gut microbial ecosystems. Int. J. Med. Microbiol. 2016;306:280–289. doi: 10.1016/j.ijmm.2016.03.007. PubMed DOI

Han J., Lin K., Sequeira C., Borchers C.H. An isotope-labeled chemical derivatization method for the quantitation of short-chain fatty acids in human feces by liquid chromatography-tandem mass spectrometry. Anal. Chim. Acta. 2015;854:86–94. doi: 10.1016/j.aca.2014.11.015. PubMed DOI

Starke R., Jehmlich N., Alfaro T., Dohnalkova A., Capek P., Bell S.L., Hofmockel K.S. Incomplete cell disruption of resistant microbes. Sci. Rep. 2019;9:5618. doi: 10.1038/s41598-019-42188-9. PubMed DOI PMC

Hughes C.S., Foehr S., Garfield D.A., Furlong E.E., Steinmetz L.M., Krijgsveld J. Ultrasensitive proteome analysis using paramagnetic bead technology. Mol. Syst. Biol. 2014;10:757. doi: 10.15252/msb.20145625. PubMed DOI PMC

Haange S.B., Jehmlich N., Hoffmann M., Weber K., Lehmann J., von Bergen M., Slanina U. Disease Development Is Accompanied by Changes in Bacterial Protein Abundance and Functions in a Refined Model of Dextran Sulfate Sodium (DSS)-Induced Colitis. J. Proteome Res. 2019;18:1774–1786. doi: 10.1021/acs.jproteome.8b00974. PubMed DOI

Käll L., Canterbury J.D., Weston J., Noble W.S., MacCoss M.J. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods. 2007;4:923–925. doi: 10.1038/nmeth1113. PubMed DOI

Kanehisa M., Sato Y., Kawashima M., Furumichi M., Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 2016;44:D457–D462. doi: 10.1093/nar/gkv1070. PubMed DOI PMC

Kanehisa M., Sato Y., Morishima K. BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences. J. Mol. Biol. 2016;428:726–731. doi: 10.1016/j.jmb.2015.11.006. PubMed DOI

Goeminne L.J., Gevaert K., Clement L. Peptide-level Robust Ridge Regression Improves Estimation, Sensitivity, and Specificity in Data-dependent Quantitative Label-free Shotgun Proteomics. Mol. Cell Proteom. 2016;15:657–668. doi: 10.1074/mcp.M115.055897. PubMed DOI PMC

Goeminne L.J.E., Gevaert K., Clement L. Experimental design and data-analysis in label-free quantitative LC/MS proteomics: A tutorial with MSqRob. J. Proteom. 2018;171:23–36. doi: 10.1016/j.jprot.2017.04.004. PubMed DOI

Bligh E.G., Dyer W.J. A Rapid Method of Total Lipid Extraction and Purification. Can. J. Biochem. Phys. 1959;37:911–917. doi: 10.1139/o59-099. PubMed DOI

Morrison W.R., Smith L.M. Preparation of Fatty Acid Methyl Esters + Dimethylacetals from Lipids with Boron Fluoride-Methanol. J. Lipid. Res. 1964;5:600–608. PubMed

Heipieper H.J., de Bont J.A. Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes. Appl. Environ. Microbiol. 1994;60:4440–4444. doi: 10.1128/AEM.60.12.4440-4444.1994. PubMed DOI PMC

Unell M., Kabelitz N., Jansson J.K., Heipieper H.J. Adaptation of the psychrotrophArthrobacter chlorophenolicusA6 to growth temperature and the presence of phenols by changes in the anteiso/iso ratio of branched fatty acids. FEMS Microbiol. Lett. 2007;266:138–143. doi: 10.1111/j.1574-6968.2006.00502.x. PubMed DOI

Kleiner M., Thorson E., Sharp C.E., Dong X., Liu D., Li C., Strous M. Assessing species biomass contributions in microbial communities via metaproteomics. Nat. Commun. 2017;8:1558. doi: 10.1038/s41467-017-01544-x. PubMed DOI PMC

Horan T.S., Pulcastro H., Lawson C., Gerona R., Martin S., Gieske M.C., Sartain C.V., Hunt P.A. Replacement Bisphenols Adversely Affect Mouse Gametogenesis with Consequences for Subsequent Generations. Curr. Biol. 2018;28:2948–2954 e2943. doi: 10.1016/j.cub.2018.06.070. PubMed DOI PMC

Eladak S., Grisin T., Moison D., Guerquin M.J., N’Tumba-Byn T., Pozzi-Gaudin S., Benachi A., Livera G., Rouiller-Fabre V., Habert R. A new chapter in the bisphenol A story: Bisphenol S and bisphenol F are not safe alternatives to this compound. Fertil. Steril. 2015;103:11–21. doi: 10.1016/j.fertnstert.2014.11.005. PubMed DOI

Liao C., Kannan K. Concentrations and profiles of bisphenol A and other bisphenol analogues in foodstuffs from the United States and their implications for human exposure. J. Agric. Food Chem. 2013;61:4655–4662. doi: 10.1021/jf400445n. PubMed DOI

Vijayalakshmi V., Senthilkumar P., Mophin-Kani K., Sivamani S., Sivarajasekar N., Vasantharaj S. Bio-degradation of Bisphenol A by Pseudomonas aeruginosa PAb1 isolated from effluent of thermal paper industry: Kinetic modeling and process optimization. J. Radiat. Res. Appl. Sci. 2019;11:56–65. doi: 10.1016/j.jrras.2017.08.003. DOI

Hamer H.M., Jonkers D., Venema K., Vanhoutvin S., Troost F.J., Brummer R.J. Review article: The role of butyrate on colonic function. Aliment. Pharmacol. Ther. 2008;27:104–119. doi: 10.1111/j.1365-2036.2007.03562.x. PubMed DOI

Nyangale E.P., Mottram D.S., Gibson G.R. Gut microbial activity, implications for health and disease: The potential role of metabolite analysis. J. Proteome Res. 2012;11:5573–5585. doi: 10.1021/pr300637d. PubMed DOI

Reddivari L., Veeramachaneni D.N.R., Walters W.A., Lozupone C., Palmer J., Hewage M.K.K., Bhatnagar R., Amir A., Kennett M.J., Knight R., et al. Perinatal Bisphenol A Exposure Induces Chronic Inflammation in Rabbit Offspring via Modulation of Gut Bacteria and Their Metabolites. mSystems. 2017;2 doi: 10.1128/mSystems.00093-17. PubMed DOI PMC

Parsons J.B., Rock C.O. Bacterial lipids: Metabolism and membrane homeostasis. Prog. Lipid. Res. 2013;52:249–276. doi: 10.1016/j.plipres.2013.02.002. PubMed DOI PMC

Bakir M.A., Kitahara M., Sakamoto M., Matsumoto M., Benno Y. Bacteroides finegoldii sp. nov., isolated from human faeces. Int. J. Syst. Evol. Microbiol. 2006;56:931–935. doi: 10.1099/ijs.0.64084-0. PubMed DOI

Sakamoto M., Ohkuma M. Bacteroides reticulotermitis sp. nov., isolated from the gut of a subterranean termite (Reticulitermes speratus) Int. J. Syst. Evol. Microbiol. 2013;63:691–695. doi: 10.1099/ijs.0.040931-0. PubMed DOI

Paek J., Shin Y., Kook J.K., Chang Y.H. Blautia argi sp. nov., a new anaerobic bacterium isolated from dog faeces. Int. J. Syst. Evol. Micr. 2019;69:33–38. doi: 10.1099/ijsem.0.002981. PubMed DOI

Park S.K., Kim M.S., Roh S.W., Bae J.W. Blautia stercoris sp. nov., isolated from human faeces. Int. J. Syst. Evol. Microbiol. 2012;62:776–779. doi: 10.1099/ijs.0.031625-0. PubMed DOI

Haack S.K., Garchow H., Odelson D.A., Forney L.J., Klug M.J. Accuracy, Reproducibility, and Interpretation of Fatty-Acid Methyl-Ester Profiles of Model Bacterial Communities. Appl. Environ. Microb. 1994;60:2483–2493. doi: 10.1128/AEM.60.7.2483-2493.1994. PubMed DOI PMC

Murinova S., Dercova K. Response mechanisms of bacterial degraders to environmental contaminants on the level of cell walls and cytoplasmic membrane. Int. J. Microbiol. 2014;2014:873081. doi: 10.1155/2014/873081. PubMed DOI PMC

Grogan D.W., Cronan J.E. Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 1997;61:429–441. doi: 10.1128/.61.4.429-441.1997. PubMed DOI PMC

Heipieper H.J., Fischer J. Bacterial Solvent Responses and Tolerance: Cis–Trans Isomerization. In: Timmis K.N., editor. Handbook of Hydrocarbon and Lipid Microbiology. Springer; Berlin/Heidelberg, Germany: 2010. pp. 4203–4211. DOI

Oh H.Y., Lee J.O., Kim O.B. Increase of organic solvent tolerance of Escherichia coli by the deletion of two regulator genes, fadR and marR. Appl. Microbiol. Biotechnol. 2012;96:1619–1627. doi: 10.1007/s00253-012-4463-8. PubMed DOI PMC

Ramos J.L., Duque E., Gallegos M.T., Godoy P., Ramos-Gonzalez M.I., Rojas A., Teran W., Segura A. Mechanisms of solvent tolerance in gram-negative bacteria. Annu. Rev. Microbiol. 2002;56:743–768. doi: 10.1146/annurev.micro.56.012302.161038. PubMed DOI

Dyrda G., Boniewska-Bernacka E., Man D., Barchiewicz K., Slota R. The effect of organic solvents on selected microorganisms and model liposome membrane. Mol. Biol. Rep. 2019;46:3225–3232. doi: 10.1007/s11033-019-04782-y. PubMed DOI

Gordeliy V.I., Kiselev M.A., Lesieur P., Pole A.V., Teixeira J. Lipid membrane structure and interactions in dimethyl sulfoxide/water mixtures. Biophys. J. 1998;75:2343–2351. doi: 10.1016/S0006-3495(98)77678-7. PubMed DOI PMC

Chang C.Y., Simon E. The effect of dimethyl sulfoxide (DMSO) on cellular systems. Proc. Soc. Exp. Biol. Med. 1968;128:60–66. doi: 10.3181/00379727-128-32943. PubMed DOI

Eberlein C., Baumgarten T., Starke S., Heipieper H.J. Immediate response mechanisms of Gram-negative solvent-tolerant bacteria to cope with environmental stress: Cis-trans isomerization of unsaturated fatty acids and outer membrane vesicle secretion. Appl. Microbiol. Biotechnol. 2018;102:2583–2593. doi: 10.1007/s00253-018-8832-9. PubMed DOI PMC

Zhang G., Meredith T.C., Kahne D. On the essentiality of lipopolysaccharide to Gram-negative bacteria. Curr. Opin. Microbiol. 2013;16:779–785. doi: 10.1016/j.mib.2013.09.007. PubMed DOI PMC

Lazarevic V., Karamata D. The tagGH operon of Bacillus subtilis 168 encodes a two-component ABC transporter involved in the metabolism of two wall teichoic acids. Mol. Microbiol. 1995;16:345–355. doi: 10.1111/j.1365-2958.1995.tb02306.x. PubMed DOI

Schirner K., Marles-Wright J., Lewis R.J., Errington J. Distinct and essential morphogenic functions for wall- and lipo-teichoic acids in Bacillus subtilis. EMBO J. 2009;28:830–842. doi: 10.1038/emboj.2009.25. PubMed DOI PMC

Neuhaus F.C., Baddiley J. A continuum of anionic charge: Structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 2003;67:686–723. doi: 10.1128/MMBR.67.4.686-723.2003. PubMed DOI PMC

Vergara-Irigaray M., Maira-Litran T., Merino N., Pier G.B., Penades J.R., Lasa I. Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface. Microbiology. 2008;154:865–877. doi: 10.1099/mic.0.2007/013292-0. PubMed DOI PMC

Paulsen I.T., Beness A.M., Saier M.H., Jr. Computer-based analyses of the protein constituents of transport systems catalysing export of complex carbohydrates in bacteria. Microbiology. 1997;143 Pt 8:2685–2699. doi: 10.1099/00221287-143-8-2685. PubMed DOI

Klein G., Raina S. Regulated Assembly of LPS, Its Structural Alterations and Cellular Response to LPS Defects. Int. J. Mol. Sci. 2019;20:356. doi: 10.3390/ijms20020356. PubMed DOI PMC

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