Abstract
DNA adduction in the model yeast Saccharomyces cerevisiae was investigated after exposure to the fungicide penconazole and the reference genotoxic compound benzo(a)pyrene, for validating yeasts as a tool for molecular toxicity studies, particularly of environmental pollution. The effect of the toxicants on the yeast’s growth kinetics was determined as an indicator of cytotoxicity. Fermentative cultures of S. cerevisiae were exposed to 2 ppm of Penconazole during different phases of growth; while 0.2 and 2 ppm of benzo(a)pyrene were applied to the culture medium before inoculation and on exponential cultures. Exponential respiratory cultures were also exposed to 0.2 ppm of B(a)P for comparison of both metabolisms. Penconazole induced DNA adducts formation in the exponential phase test; DNA adducts showed a peak of 54.93 adducts/109 nucleotides. Benzo(a)pyrene induced the formation of DNA adducts in all the tests carried out; the highest amount of 46.7 adducts/109 nucleotides was obtained in the fermentative cultures after the exponential phase exposure to 0.2 ppm; whereas in the respiratory cultures, 14.6 adducts/109 nucleotides were detected. No cytotoxicity was obtained in any experiment. Our study showed that yeast could be used to analyse DNA adducts as biomarkers of exposure to environmental toxicants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.
References
Abdulovic AL, Jinks-Robertson S (2006) The in vivo characterization of translesion synthesis across UV-induced lesions in Saccharomyces cerevisiae: insights into Pol zeta- and Pol eta-dependent frameshift mutagenesis. Genetics 172(3):1487–1498. https://doi.org/10.1534/genetics.105.052480
Albertini S (1991) Reevaluation of the 9 compounds reported conclusive positive in yeast Saccharomyces cerevisiae aneuploidy test systems by the Gene-Tox Program using strain D61.M of Saccharomyces cerevisiae. Mutat Res 260(2):165–180. https://doi.org/10.1016/0165-1218(91)90005-7
Allaf MM, Trick CG (2021) Yeast cell as a bio-model for measuring the toxicity of fish-killing flagellates. Toxins 13:821. https://doi.org/10.3390/toxins13110821
Amat-Bronnert A, Castegnaro M, Pfohl-Leszkowicz A (2007) Genotoxic activity and induction of biotransformation enzymes in two human cell lines after treatment by Erika fuel extract. Environ Toxicol Pharmacol 23(1):89–95. https://doi.org/10.1016/j.etap.2006.07.006
Ballatori N, Villalobos AR (2002) Defining the molecular and cellular basis of toxicity using comparative models. Toxicol Appl Pharmacol 183(3):207–220. https://doi.org/10.1006/taap.2002.9488
Baynton K, Bresson-Roy A, Fuchs RPP (1998) Analysis of damage tolerance pathways in Saccharomyces cerevisiae: a requirement for Rev3 DNA polymerase in translesion synthesis. Mol Cell Biol 18(2):960–966. https://doi.org/10.1128/mcb.18.2.960
Bedard LL, Massey TE (2006) Aflatoxin B1-induced DNA damage and its repair. Cancer Lett 241(2):174–183. https://doi.org/10.1016/j.canlet.2005.11.018
Bharadwaj P, Martins R (2020) A rapid absorbance-based growth assay to screen the toxicity of oligomer Aβ42 and protect against cell death in yeast. Neural Regen Res 15(10):1931–1936. https://doi.org/10.4103/1673-5374.280318
Bhattacharya SS, Syed K, Shann JR, Yadav JS (2013) A novel P450-initiated biphasic process for sustainable biodegradation of benzo[a]pyrene in soil under nutrient-sufficient conditions by the white rot fungus Phanerochaete chrysosporium. J Hazard Mater 261:675–683. https://doi.org/10.1016/j.jhazmat.2013.07.055
Braconi D, Bernardini G, Santucci A (2016) Saccharomyces cerevisiae as a model in ecotoxicological studies: a post-genomics perspective. J Proteomics 137:19–34. https://doi.org/10.1016/j.jprot.2015.09.001
Bressler J, Maertens A, Locke P (2018) Alternative Testing models for testing chemical toxicity. Compreh Toxicol (third Edition) 9:119–126
Cabral MG, Viegas CA, Teixeira MC, Sá-Correia I (2003) Toxicity of chlorinated phenoxyacetic acid herbicides in the experimental eukaryotic model Saccharomyces cerevisiae: role of pH and of growth phase and size of the yeast cell population. Chemosphere 51:47–54. https://doi.org/10.1016/s0045-6535(02)00614-8
Callen DF, Wolf CR, Philpot RM (1980) Cytochrome P-450 mediated genetic activity and cytotoxicity of seven halogenated aliphatic hydrocarbons in Saccharomyces cerevisiae. Mutat Res 77(1):55–63. https://doi.org/10.1016/0165-1218(80)90120-2
Canova S, Viezzer C, Venier P, Navazio L, Revoltella R, Celotti L (1996) Metabolic activation of benzo[a]pyrene in two fetal mouse hepatocyte lines: induction of DNA adducts and micronuclei. Mutat Res 367(3):135–141. https://doi.org/10.1016/0165-1218(95)00086-0
Cerniglia CE (1984) Microbial metabolism of polycyclic aromatic hydrocarbon. Adv Appl Microbiol 30:31–71. https://doi.org/10.1016/s0065-2164(08)70052-2
Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbon. Biodegradation 3:351–368
Cerniglia CE, Crow SA (1981) Metabolism of aromatic hydrocarbons by yeasts. Arch Microbiol 129:9–13
Châtel A, Faucet-Marquis V, Perret M, Gourlay-Francé C, Uhrer E, Pfohl-Leszkowicz A, Vincent-Hubert F (2012) Genotoxicity assessment and detoxification induction in Dreissena polymorpha exposed to benzo[a]pyrene. Mutagenesis 27(6):703–711. https://doi.org/10.1093/mutage/ges036
Dallinga JW, Pachen DM, Wijnhoven SW, Breedijk A, Van’t Veer L, Wigbout G, van Zandwijk N, Maas LM, van Agen E, Kleinjans JC, van Schooten FJ (1998) The use of 4-aminobiphenyl haemoglobin adducts and aromatic DNA adducts in lymphocytes of smokers as biomarkers of exposure. Cancer Epidemiol Biomarkers Prev 7:571–577
Delia-Dupuy ML, Strehaiano P (1996) La fermentation alcoolique en vinification: observations cinétiques et physiologie. Revue Française D’œnologie 159:19–23
Dolinski K, Botstein D (2005) Changing perspectives in yeast research nearly a decade after the genome sequence. Genome Res 15:1611–1619. https://doi.org/10.1101/gr.3727505
Fasullo M, Sun M, Egner P (2008) Stimulation of sister chromatid exchanges and mutation by aflatoxin B1-DNA adducts in Saccharomyces cerevisiae requires MEC1 (ATR), RAD53, and DUN1. Mol Carcinog 47(8):608–615. https://doi.org/10.1002/mc.20417
Fasullo M, Smith A, Egner P, Cera C (2014) Activation of aflatoxin B1 by expression of human CYP1A2 polymorphisms in Saccharomyces cerevisiae. Mutat Res—Genet Toxicol Environ Mutagen 76:18–26. https://doi.org/10.1016/j.mrgentox.2014.01.009
Fasullo M, Freedland J, St John N, Cera C, Egner P, Hartog M, Ding X (2017) An in vitro system for measuring genotoxicity mediated by human CYP3A4 in Saccharomyces cerevisiae. Environ Mol Mutagen 58(4):217–227. https://doi.org/10.1002/em.22093
Faucet V, Pfohl-Leszkowicz A, Dai J, Castegnaro M, Manderville R (2004) Evidence for covalent DNA adduction by ochratoxin A following chronic exposure to rat and subacute exposure to pig. Chem Res Toxicol 17:1289–1296. https://doi.org/10.1021/tx049877s
Faucet V (2005) L’ochratoxine A, contaminant alimentaire, est-elle un cancérogène génotoxique ou épigénétique ? Recherche des effets génotoxiques par la technique de post-marquage de l’ADN au 32P en relation avec la métabolisation de l’ochratoxine A. PhD diss. Institut National Polytechnique de Toulouse
Fujita K, Nagaoka M, Komatsu Y, Iwahashia H (2003) Yeast pheromone signaling pathway as a bioassay to assess the effect of chemicals on mammalian peptide hormones. Ecotoxicol Environ Saf 56:358–366. https://doi.org/10.1016/s0147-6513(02)00116-1
Gadaleta MC, Iwasaki O, Noguchi C, Noma K, Noguchi E (2015) Chromatin immunoprecipitation to detect DNA replication and repair factors. Methods Mol Biol 1300:169–186. https://doi.org/10.1007/978-1-4939-2596-4_12
Gilberson T, Peluso ME, Munia A, Luján-Barroso L, Sánchez MJ, Navarro C, Amiano P, Barricarte A, Quirós JR, Molina-Montes E et al (2014) Aromatic adducts and lung cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) Spanish cohort. Carcinogenesis 35(9):2047–2054. https://doi.org/10.1093/carcin/bgu098
Girard P-M, Guibourt N, Boiteux S (1997) The Ogg1 protein of Saccharomyces cerevisiae: a 7,8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity. Nucleic Acids Res 25(16):3204–3211. https://doi.org/10.1093/nar/25.16.3204
Girard PM, D’Ham C, Cadet J, Boiteux S (1998) Opposite base-dependant excision of 7,8-dihydro-8-oxoadenine by the Ogg1 protein of Saccharomyces cerevisiae. Carcinogenesis 19(7):1299–1305. https://doi.org/10.1093/carcin/19.7.1299
Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M et al (1996) Life with 6000 genes. Science 274(5287):546–567. https://doi.org/10.1126/science.274.5287.546
Goin CJ, Mayer VW (1995) Induction of chromosome loss in Saccharomyces cerevisiae strain D61.M by selected benzimidazole compounds. Mutat Res 343:185–199. https://doi.org/10.1016/0165-1218(95)90014-4
Guengerich FP (2001) Forging the links between metabolism and carcinogenesis. Mutat Res 488:195–209. https://doi.org/10.1016/s1383-5742(01)00059-x
Guo Y, Breeden LL, Zarbl H, Preston BD, Eaton DL (2005) Expression of a human cytochrome P450 in yeast permits analysis of pathways for response to and repair of aflatoxin-induced DNA damage. Mol Cell Biol 25(14):5823–5833. https://doi.org/10.1128/MCB.25.14.5823-5833.2005
Guo Y, Breeden LL, Fan W, Zhao PL, Eaton DL, Zarbl H (2006) Analysis of cellular responses to aflatoxin B1 in yeast expressing human cytochrome P450 1A2 using cDNA microarrays. Mutat Res 593(1–2):121–142. https://doi.org/10.1016/j.mrfmmm.2005.07.001
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169(1–3):1–15. https://doi.org/10.1016/j.jhazmat.2009.03.137
Hemminki K (1995) DNA adducts in biomonitoring. Toxicol Lett 77:227–229. https://doi.org/10.1016/0378-4274(95)03299-1
Hesham A-L, Wang Z, Zhang Y, Zhang J, Wenzhou LV, Yang M (2006) Isolation and identification of a yeast strain capable of degrading four and five ring aromatic hydrocarbons. Ann Microbiol 56(2):109–112
Hesham A-L, Khan S, Tao Y, Li D, Zhang Y, Yang M (2012) Biodegradation of high molecular weight PAHs using isolated yeast mixtures: application of meta-genomic methods for community structure analyses. Environ Sci Pollut Res 19(8):3568–3578. https://doi.org/10.1007/s11356-012-0919-8
Jawich D (2006) Etude de la toxicité de pesticides vis-à-vis de deux genres de levures: approche cinétique et moléculaire. Université Saint Joseph de Beyrouth, Institut National Polytechnique de Toulouse, PhD diss
Jawich D, Lteif R, Pfohl-Leszkowicz A, Strehaiano P (2006) Effects of penconazole on two yeast strains: growth kinetics and molecular studies. Mol Nutr Food Res 50(6):552–556. https://doi.org/10.1002/mnfr.200500213
Johnson RE, Yu SL, Prakash S, Prakash L (2007) A role for yeast and human translesion synthesis DNA polymerases in promoting replication through 3-methyl adenine. Mol Cell Biol 27(20):7198–7205. https://doi.org/10.1128/MCB.01079-07
Kadri T, Rouissi T, Kaur Brar S, Cledon M, Sarma S, Verma M (2017) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungal enzymes: a review. J Environ Sci 51:52–74. https://doi.org/10.1016/j.jes.2016.08.023
Keller-Seitz MU, Certa U, Sengstag C, Wurgler FE, Sun M, Fasullo M (2004) Transcriptional response of yeast to aflatoxin B1: recombinational repair involving RAD51 and RAD1. Mol Biol Cell 15(9):4321–4336. https://doi.org/10.1091/mbc.E04-05-0375
Kim YH, Ahn JY, Moon SH, Lee J (2005) Biodegradation and detoxification of organophosphate insecticide, malathion by Fusarium oxysporum f. sp. pisi cutinase. Chemosphere 60(10):1349–1355. https://doi.org/10.1016/j.chemosphere.2005.02.023
King DJ, Wiseman A (1987) Yeast cytochrome P-448 enzymes and the activation of mutagens, including carcinogens. In: Wiseman A (ed) Enzyme induction, mutagen activation and carcinogen testing in yeast. Ellis Horwood, Chichester, pp 115–167
Knight AW, Keenan PO, Goddard NJ, Fielden PR, Walmsley RM (2004) A yeast-based cytotoxicity and genotoxicity assay for environmental monitoring using novel portable instrumentation. J Environ Monit 6(1):71–79. https://doi.org/10.1039/b310206h
Koch R, Schlegelmilch R, Wolf HU (1988) Genetic effects of chlorinated ethylenes in the yeast Saccharomyces cerevisiae. Mutat Res 206(2):209–216. https://doi.org/10.1016/0165-1218(88)90162-0
Kong SE, Svejstrup JQ (2002) Incision of a 1,3-intrastrand d(GpTpG)-cisplatin adduct by nucleotide excision repair proteins from yeast. DNA Repair 1(9):731–741. https://doi.org/10.1016/s1568-7864(02)00080-0
Krasikova YS, Rechkunova NI, Maltseva EA, Pestryakov PE, Petruseva IO, Sugasawa K, Chen X, Min JH, Lavrik OI (2013) Comparative analysis of interaction of human and yeast DNA damage recognition complexes with damaged DNA in nucleotide excision repair. J Biol Chem 288(15):10936–10947. https://doi.org/10.1074/jbc.M112.444026
Lee HJ, Gu MB (2003) Effect of benzo(a)pyrene on genes related to the cell cycle cytochrome P450 of Saccharomyces cerevisiae. J Microbiol Biotechnol 13(4):624–627
Mandal SK, Selvi A, Das N (2016) A novel approach on degradation of Benzo[a]pyrene by yeast consortium isolated from contaminated soil. Der Pharm Lett 8(7):80–93
Marinovska P, Todorova T, Tomova A, Pisareva E, Boyadzhiev K, Dimitrov M, Parvanova P, Dimitrova M, Chankova S, Petrova V (2022) Saccharomyces cerevisiae yeast cells as a test system for assessing Zeocin toxicity. BioRisk 17:105–116. https://doi.org/10.3897/biorisk.17.77227
Masfaraud JF, Devaux A, Pfohl-Leszkowicz A, Malaveille C, Monod G (1992) DNA adduct formation and EROD induction in primary culture of rainbow trout hepatocytes exposed to benzo(a)pyrene. Toxicol in Vitro 6(6):523–531. https://doi.org/10.1016/0887-2333(92)90064-X
Mattiazzi M, Petrovič U, Križaj I (2012) Yeast as a model eukaryote in toxinology: a functional genomics approach to studying the molecular basis of action of pharmacologically active molecules. Toxicon 60(4):558–571. https://doi.org/10.1016/j.toxicon.2012.03.014
McKinney JS, Sethi S, Tripp JD, Nguyen TN, Sanderson BA, Westmoreland JW, Resnick MA, Lewis LK (2013) A multistep genomic screen identifies new genes required for repair of DNA double-strand breaks in Saccharomyces cerevisiae. BMC Genom 14:Article number 251. https://doi.org/10.1186/1471-2164-14-251
Mueller JG, Cerniglia CE, Pritchard PH (1996) Bioremediation of environments contaminated by polycyclic aromatic hydrocarbons. Bioremediation principles and applications. Cambridge University Press, pp 125–194
Munnia A, Giese RW, Polvani S, Galli A, Cellai F, Peluso MEM (2017) Bulky DNA adducts, tobacco smoking, genetic susceptibility, and lung cancer risk. Adv Clin Chem 81:231–277. https://doi.org/10.1016/bs.acc.2017.01.006
O’Connor STF, Lan J, North M, Loguinov A, Zhang L, Smith MT, Gu AZ, Vulpe C (2013) Genome-wide functional and stress response profiling reveals toxic mechanism and genes required for tolerance to benzo[a]pyrene in S. cerevisiae. Front Genet/toxicogenomics 3(316):1–20. https://doi.org/10.3389/fgene.2012.00316
Pereira C, Martins LM, Saraiva L (2014) LRRK2, but not pathogenic mutants, protects against H2O2 stress depending on mitochondrial function and endocytosis in a yeast model. Biochim Biophys Acta 1840(6):2025–2031. https://doi.org/10.1016/j.bbagen.2014.02.015
Pfohl-Leszkowicz A (1994) Effet des cancérogènes sur la méthylation biologique de l’ADN et détection des adduits à l’ADN. Regard Sur La Biochimie 3:51–61
Pfohl-Leszkowicz A (2008) Formation, persistence and significance of DNA adduct formation in relation to some pollutants from a broad perspective. Adv Mol Toxicol 2:183–239. https://doi.org/10.1016/S1872-0854(07)02007-3
Pfohl-Leszkowicz A (2009) Ochratoxin A and aristolochic acid involvement in nephropathies and associated urothelial tract tumours. Arch Ind Hyg Toxicol 60(4):465–483. https://doi.org/10.2478/10004-1254-60-2009-2000
Pfohl-Leszkowicz A, Castegnaro M (2005) Further arguments in favour of direct covalent binding of Ochratoxin A (OTA) after metabolic biotransformation. Food Addit Contam 22:75–87. https://doi.org/10.1080/02652030500309400
Pfohl-Leszkowicz A, Chakor K, Creppy EE, Dirheimer G (1991) DNA-adducts formation and variation of DNA-methylation after treatment of mice with ochratoxin A. In: Castegnaro M, Plestina R, Dirheimer G, Chernozemsky IN, Bartsch H (eds) Mycotoxins, endemic nephropathy and urinary tracts tumours, vol 115. IARC Scientific Publications, Lyon, pp 245–253
Pfohl-Leszkowicz A, Masfaraud JF, Weber-Lotfi F, Marty J, Guillemaut P, Castegnaro M (1996) Comparison of animal and plant DNA-adducts after exposure to benzo(a)pyrene. Polycycl Aromat Compd 10:323–331. https://doi.org/10.1080/10406639608034713
Pfohl-leszkowicz A, Guerre P, Galtier P (1999) Métabolisation des mycotoxines In: Les mycotoxines dans l’alimentation: évaluation et gestion du risqué. Tec & Doc, pp. 37–68
Pizzul P, Casari E, Gnugnoli M, Rinaldi C, Corallo F, Longhese MP (2022) The DNA damage checkpoint: a tale from budding yeast. Front Genet 13:995163. https://doi.org/10.3389/fgene.2022.995163
Plakos K, DeRose VJ (2017) Mapping platinum adducts on yeast ribosomal RNA using high-throughput sequencing. ChemComm 53(95):12746–12749. https://doi.org/10.1039/c7cc06708a
Prakash S, Prakash L (2000) Nucleotide excision repair in yeast. Mutat Res 451:13–24. https://doi.org/10.1016/s0027-5107(00)00037-3
Reddy MV, Randerath K (1986) Nuclease P1 mediated enhancement sensitivity of 32-P-postlabeling test for structurally diverse DNA adducts. Carcinogenesis 7(9):1543–1551. https://doi.org/10.1093/carcin/7.9.1543
Rether B, Pfohl-Leszkowicz A, Guillemaut P, Keith G (1990) Benzo(a)pyrene induces nuclear DNA adducts in plant cell suspension culture: detection by 32P postlabelling. FEBS Lett 236(1):172–174. https://doi.org/10.1016/0014-5793(90)80732-X
Ribeiro IC, Verissimo I, Moniz L, Cardoso H, Sousa MJ, Soares AM, Leão C (2000) Yeasts as a model for assessing the toxicity of the fungicides penconazole, cymoxanil and dichlofluanid. Chemosphere 41(10):1637–1642. https://doi.org/10.1016/s0045-6535(00)00039-4
Ricceri F, Godschalk RW, Peluso M, Phillips DH, Agudo A, Georgiadis P, Loft S, Tjonneland A, Raaschou-Nielsen O, Palli D et al (2010) Bulky DNA adducts in white blood cells: a pooled analysis of 3,600 subjects. Cancer Epidemiol Biomarkers Prev 19(12):3174–3181. https://doi.org/10.1158/1055-9965.EPI-10-0314
Rodriguez CE, Shinyashiki M, Froines J, Yu RC, Fukuto JM, Cho AK (2004) An examination of quinone toxicity using the yeast Saccharomyces cerevisiae model system. Toxicology 201(1–3):185–196. https://doi.org/10.1016/j.tox.2004.04.016
Romero MC, Urrutia MI, Reinoso HE, Kiernan MM (2010) Benzo[a]pyrene degradation by soil filamentous fungi. J Yeast Fungal Res 1(2):025–029. https://doi.org/10.5897/JYFR.9000008
Rossner P, Svecova V, Schmuczerova J, Milcova A, Tabashidze N, Topinka J, Pastorkova A, Sram RJ (2013) Analysis of biomarkers in a Czech population exposed to heavy air pollution: part I—bulky DNA adducts. Mutagenesis 28(1):89–95. https://doi.org/10.1093/mutage/ges057
Saffran WA, Ahmed A, Binyaminov O, Gonzalez C, Gupta A, Fajardo MA, Kishun D, Nandram A, Reyes K, Scalercio K, Senior CW (2014) Induction of direct repeat recombination by psoralen-DNA adducts in Saccharomyces cerevisiae: defects in DNA repair increase gene copy number variation. DNA Repair 21:87–96. https://doi.org/10.1016/j.dnarep.2014.05.011
Saint-Denis M, Pfohl-Leszkowicz A, Narbonne JF, Ribera D (2000) Dose-response and kinetics of the formation of DNA adducts in the earthworm eisenia fetida andrei exposed to B(A)P-contaminated artificial soil. Polycycl Aromat Compd 18(2):117–127. https://doi.org/10.1080/10406630008028140
Salmon JM, Fornairon C, Barre P (1998) Determination of oxygen utilization pathways in an industrial strain of Saccharomyces cerevisiae during enological fermentation. J Ferment Bioeng 86(2):154–163. https://doi.org/10.1016/s0922-338x(98)80054-8
Schafer B, Neffgen A, Klinner U (2008) A novel yeast-based tool to detect mutagenic and recombinogenic effects simultaneously. Mutat Res—Genet Toxicol Environ Mutagen 652(1):20–29
Schilderman PA, Moonen EJ, Maas LM, Welle I, Kleinjans JC (1999) Use of crayfish in biomonitoring studies of environmental pollution of the river Meuse. Ecotoxicol Environ Saf 44:241–252. https://doi.org/10.1006/eesa.1999.1827
Shin J, Kim JE, Lee YW, Son H (2018) Fungal cytochrome P450s and the P450 complement (CYPome) of Fusarium graminearum. Toxins 10(3):112. https://doi.org/10.3390/toxins10030112
Shivange G, Kodipelli N, Monisha M, Anindya R (2014) A role for Saccharomyces cerevisiae Tpa1 protein in direct alkylation repair. J Biol Chem 289(52):35939–35952. https://doi.org/10.1074/jbc.M114.590216
Simhadri S, Kramata P, Zajc B, Sayer JM, Jerina DM, Hinkle DC, Wei CS (2002) Benzo[a]pyrene diol epoxide-deoxyguanosine adducts are accurately bypassed by yeast DNA polymerase zeta in vitro. Mutat Res 508(1–2):137–145. https://doi.org/10.1016/S0027-5107(02)00211-7
Sohn HY, Kwon CS, Kwon GS, Lee JB, Kim E (2004) Induction of oxidative stress by endosulfan and protective effect of lipid-soluble antioxidants against endosulfan-induced oxidative damage. Toxicol Lett 151:357–365. https://doi.org/10.1016/j.toxlet.2004.03.004
Stone JE, Kumar D, Binz SK, Inase A, Iwai S, Chabes A, Burgers PM, Kunkel TA (2011) Lesion bypass by S. cerevisiae Pol ζ alone. DNA Repair 10(8):826–834. https://doi.org/10.1016/j.dnarep.2011.04.032
Strehaiano P (1984) Phénomènes d’inhibition en fermentation alcoolique : observations cinétiques. PhD diss., Institut National Polytechnique de Toulouse
Sutherland JB (1992) Detoxification of polycyclic aromatic hydrocarbons by fungi. J Ind Microbiol 9(1):53–61. https://doi.org/10.1007/BF01576368
Syed K, Doddapaneni H, Subramanian V, Lam YW, Yadav JS (2010) Genome-to-function characterization of novel fungal P450 monooxygenases oxidizing polycyclic aromatic hydrocarbons (PAHs). Biochem Biophys Res Commun 399(4):492–497. https://doi.org/10.1016/j.bbrc.2010.07.094
Takahashi T (2011) Studies on molecular mechanism of toxicity of anticancer drugs. Yakugaku Zasshi: J Pharma Soc Jpn 131(3):355–358. https://doi.org/10.1248/yakushi.131.355
Teixeira MC, Duque P, Sá-Correia I (2007) Environmental genomics: mechanistic insights into toxicity of and resistance to the herbicide 2,4-D. Trends Biotechnol 25(8):363–370. https://doi.org/10.1016/j.tibtech.2007.06.002
Torres E, Sandoval JV, Resell FI, Grant MA, Vazquez-Duhalt R (1995) Site-directed mutagenesis improves the biocatalytic activity of iso-1-cytochrome c in polycyclic hydrocarbon oxidation. Enzyme Microb Technol 17(11):1014–1020. https://doi.org/10.1016/0141-0229(95)00032-1
Ueda M, Kinoshita H, Yoshida T, Kamasawa N, Osumi M, Tanaka A (2003) Effect of catalase-specific inhibitor 3-amino-1,2,4-triazole on yeast peroxisomal catalase in vivo. FEMS Microbiol Lett 219:93–98. https://doi.org/10.1016/S0378-1097(02)01201-6
Vainio H (2001) Use of biomarkers in risk assessment. Int J Hyg Environ Health 204(2–3):91–102. https://doi.org/10.1078/1438-4639-00088
van Koten-Vermeulen JEM, den Tonkelaar EM (1992) Penconazole: pesticide residues in food—1992 evaluations Part II toxicology. International Programme on Chemical Safety (IPCS INCHEM), World Health Organization
Van Leeuwen JS, Vermeulen NPE, Vos JC (2012) Yeast as a humanized model organism for biotransformation-related toxicity. Curr Drug Metab 13(10):1464–1475. https://doi.org/10.2174/138920012803762783
Wang JS, Groopman JD (1999) DNA damage by mycotoxins. Mutat Res 424(1–2):167–181. https://doi.org/10.1016/s0027-5107(99)00017-2
Wang X, Yin C, Wang L (2002) Structure–activity relationships and response–surface analysis of nitroaromatics toxicity to the yeast (Saccharomyces cerevisiae). Chemosphere 46:1045–1051. https://doi.org/10.1016/s0045-6535(01)00148-5
Wang C, Liu H, Li J, Sun H (2014) Degradation of PAHs in soil by Lasiodiplodia theobromae and enhanced benzo[a]pyrene degradation by the addition of Tween-80. Environ Sci Pollut Res 21(18):10614–10625. https://doi.org/10.1007/s11356-014-3050-1
Wiseman A, Woods LFJ (1979) Benzo(a)pyrene metabolites formed by the action of yeast cytochrome P-450/P-448. J Chem Technol Biotechnol 29(5):320–324. https://doi.org/10.1002/jctb.503290508
Wiseman A, Lim TK, Woods LFJ (1978) Regulation of the biosynthesis of cytochrome P-450 in brewers [sic] yeast: role of cyclic AMP. Biochim Biophys Acta 544(3):615–623. https://doi.org/10.1016/0304-4165(78)90335-5
Woods LFJ, Wiseman A (1979) Metabolism of Benzo[a]pyrene by the cytochrome P-450/P-448 of Saccharomyces cerevisiae. Biochem Soc Trans 7(1):124–127. https://doi.org/10.1042/bst0070124
Woods LFJ, Wiseman A (1980) Benzo(a)pyrene hydroxylase from Saccharomyces cerevisiae: substrate binding, spectral and kinetic data. Biochim Biophys Acta Enzymol 613(1):52–61. https://doi.org/10.1016/0005-2744(80)90191-6
Xie Z, Braithwaite E, Guo D, Zhao B, Geacintov NE, Wang Z (2003) Mutagenesis of benzo[a]pyrene diol epoxide in yeast: requirement for DNA polymerase ζ and involvement of DNA polymerase η. Biochemistry 42(38):11253–11262. https://doi.org/10.1021/bi0346704
Yang Q, Zhang H, Li X, Wang Z, Xu Y, Ren S, Chen X, Xu Y, Hao H, Wang H (2013) Extracellular enzyme production and phylogenetic distribution of yeasts in wastewater treatment systems. Bioresour Technol 129:264–273. https://doi.org/10.1016/j.biortech.2012.11.101
Zaripov SA, Naumov AV, Abdrakhmanova JF, Garusov AV, Naumova RP (2002) Models of 2,4,6-trinitrotoluene (TNT) initial conversion by yeasts. FEMS Microbiol Lett 217:213–217. https://doi.org/10.1111/j.1574-6968.2002.tb11477.x
Acknowledgements
The authors thank the Research Council of Saint Joseph University of Beirut and the Laboratoire de Génie Chimique UMR-CNRS/INPT/UPS 5503 for the financial support.
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
Annie Pfohl-Leszkowicz and Pierre Strehaiano designed the study. Roger Lteif set up the collaboration between Lebanon and France. Dalal Jawich carried out the microbial cultures in Pierre Strehaiano and Roger Lteif teams, and DNA adducts analysis in Annie Pfohl-Leszkowicz team. Dalal Jawich analysed the data and prepared draft figures and tables. Dalal Jawich prepared the manuscript draft with important proofreading from Annie Pfohl-Leszkowicz, Pierre Strehaiano, and Roger Lteif. All authors approved the final manuscript and had complete access to the study data.
Corresponding author
Ethics declarations
Competing interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval
All authors have approved the manuscript and agree with its submission to World Journal of Microbiology and Biotechnology. We confirm that this work is original and has not been published elsewhere, nor is it currently under consideration for publication elsewhere.
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Jawich, D., Pfohl-Leszkowicz, A., Lteif, R. et al. DNA adduct formation in Saccharomyces cerevisiae following exposure to environmental pollutants, as in vivo model for molecular toxicity studies. World J Microbiol Biotechnol 40, 180 (2024). https://doi.org/10.1007/s11274-024-03989-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-024-03989-x