Comparative Toxigenicity and Associated Mutagenicity of Aspergillus fumigatus and Aspergillus flavus Group Isolates Collected from the Agricultural Environment
Abstract
:1. Introduction
2. Results
2.1. Mycotoxin Production
2.2. Mutagenicity of Fungal Extracts
2.2.1. Aspergillus flavus Extracts
2.2.2. Aspergillus parasiticus Extract
2.2.3. Aspergillus fumigatus Extract
2.3. Mutagenicity of the Mycotoxin Mixtures
2.4. Mutagenicity of Pure Mycotoxins
3. Discussion
- (a)
- the most powerful and classically described towards TA98 and TA100 upon addition of S9mix involves CYPs in the formation of reactive intermediates such as AFB1-exo-8,9-epoxide, and the subsequent binding to the N7 guanine in DNA to form AFB1-N7-Gua adducts then, subsequently, the imidazole ring-opened form AFB1-FapyGua, this latter being more mutagenic than the former [25,26];
- (b)
- a direct mutagenicity towards these two strains, observed for higher doses of mycotoxins, that did not involve any exogenously activated intermediates;
- (c)
- and a mechanism detected in TA102 for the three extracts only upon addition of S9mix, could potentially be subsequent to oxidative damage, since TA102 is responsive to this kind of damage [27].
4. Conclusions
5. Materials and Methods
5.1. Strain Collection
5.2. Toxigenic Ability of Fungal Isolates
5.3. Mutagenicity
5.3.1. Extract Preparation
5.3.2. Mixture of Mycotoxins
5.3.3. Ames Test Procedure
5.4. Statistical Analysis
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Richard, E.; Heutte, N.; Sage, L.; Pottier, D.; Bouchart, V.; Lebailly, P.; Garon, D. Toxigenic fungi and mycotoxins in mature corn silage. Food Chem. Toxicol. 1997, 45, 2420–2425. [Google Scholar] [CrossRef] [PubMed]
- Lanier, C.; Heutte, N.; Richard, E.; Bouchart, V.; Lebailly, P.; Garon, D. Mycoflora and mycotoxin production in oilseed cakes during farm storage. J. Agric. Food Chem. 2009, 57, 1640–1645. [Google Scholar] [CrossRef] [PubMed]
- Lanier, C.; Richard, E.; Heutte, N.; Picquet, R.; Bouchart, V.; Garon, D. Airborne molds and mycotoxins associated with handling of corn silage and oilseed cakes in agricultural environment. Atmos. Environ. 2010, 44, 1980–1986. [Google Scholar] [CrossRef]
- Lanier, C.; André, V.; Heutte, N.; El Kaddoumi, A.; Bouchart, V.; Picquet, R.; Garon, D. Recurrence of stachybotrys chartarum during mycological and toxicological study of bioaerosols collected in a dairy cattle shed. Ann. Agric. Environ. Med. 2012, 19, 61–67. [Google Scholar]
- Richard, J.L. Some major mycotoxins and their mycotoxicoses—An overview. Int. J. Food Microbiol. 2007, 119, 3–10. [Google Scholar] [CrossRef]
- Wang, J.S.; Groopman, J.D. DNA damage by mycotoxins. Mutat. Res. 1999, 424, 167–181. [Google Scholar] [CrossRef]
- Marchese, S.; Polo, A.; Ariano, A.; Velotto, S.; Costantini, S.; Severino, L. Aflatoxin B1 and M1: Biological Properties and Their Involvement in Cancer Development. Toxins 2018, 10, 214. [Google Scholar] [CrossRef] [Green Version]
- Theumer, M.G.; Henneb, Y.; Khoury, L.; Snini, S.P.; Tadrist, S.; Canlet, C.; Puel, O.; Oswald, I.P.; Audebert, M. Genotoxicity of aflatoxins and their precursors in human cells. Toxicol. Lett. 2018, 287, 100–107. [Google Scholar] [CrossRef]
- McCullough, A.K.; Lloyd, R.S. Mechanisms underlying aflatoxin-associated mutagenesis—Implications in carcinogenesis. DNA Repair 2019, 77, 76–86. [Google Scholar] [CrossRef]
- World Health Organization; International Agency for Research on Cancer. Aflatoxins. In IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans; IARC Press: Lyon, France, 1993; Volume 56, pp. 245–395. [Google Scholar]
- Nieminen, S.M.; Mäki-Paakkanen, J.; Hirvonen, M.R.; Roponen, M.; von Wright, A. Genotoxicity of gliotoxin, a secondary metabolite of Aspergillus fumigatus, in a battery of short-term test systems. Mutat. Res. 2002, 520, 161–170. [Google Scholar] [CrossRef]
- Stanimirovic, Z.; Stevanovic, J.; Bajic, V.; Radovic, I. Evaluation of genotoxic effects of fumagillin by cytogenetic tests in vivo. Mutat. Res. 2007, 628, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Stevanovic, J.; Stanimirovic, Z.; Radakovic, M.; Stojic, V. In vitro evaluation of the clastogenicity of fumagillin. Environ. Mol. Mutagen. 2008, 49, 594–601. [Google Scholar] [CrossRef] [PubMed]
- Sabater-Vilar, M.; Nijmeijer, S.; Fink-Gremmels, J. Genotoxicity assessment of five tremorgenic mycotoxins (Fumitremorgen B, Paxilline, Penitrem A, Verruculogen, and Verrucosidin) produced by molds isolated from fermented meats. J. Food Prot. 2003, 66, 2123–2129. [Google Scholar] [CrossRef] [PubMed]
- Bjeldanes, L.F.; Chang, G.W.; Thomson, S.V. Detection of mutagens produced by fungi with the Salmonella typhimurium assay. Appl. Environ. Microbiol. 1978, 35, 1150–1154. [Google Scholar] [CrossRef] [Green Version]
- Uka, V.; Moore, G.; Arroyo-Manzanares, N.; Nebija, D.; De Saeger, S.; Di Mavungu, J. Secondary metabolite dereplication and phylogenetic analysis identify various emerging mycotoxins and reveal the high intra-species diversity in Aspergillus flavus. Front. Microbiol. 2019, 10, 667–687. [Google Scholar] [CrossRef] [Green Version]
- Loarca-Piña, G.; Kuzmicky, P.A.; de Mejía, E.G.; Kado, N.Y. Inhibitory effects of ellagic acid on the direct-acting mutagenicity of aflatoxin B1 in the Salmonella microsuspension assay. Mutat. Res. 1998, 398, 183–187. [Google Scholar] [CrossRef]
- Bjeldanes, L.F.; Thomson, S.V. Mutagenic activity of Fusarium moniliforme isolates in the Salmonella typhimurium assay. Appl. Environ. Microbiol. 1979, 37, 1118–1121. [Google Scholar] [CrossRef] [Green Version]
- Wong, J.J.; Hsieh, D.P. Mutagenicity of aflatoxins related to their metabolism and carcinogenic potential. Proc. Natl. Acad. Sci. USA 1976, 73, 2241–2244. [Google Scholar] [CrossRef] [Green Version]
- Nakazato, M.; Saito, K.; Kikuchi, Y.; Ibe, A.; Fujinuma, K.; Nishijima, M.; Nishima, T.; Morozumi, S.; Wauke, T.; Hitokoto, H. Aflatoxicol formation by Aspergillus flavus and A. parasiticus. J. Food Hyg. Soc. Jpn. 1985, 26, 380–384. [Google Scholar] [CrossRef]
- Nakazato, M.; Morozumi, S.; Saito, K.; Fujinuma, K.; Nishima, T.; Kasai, N. Interconversion of Aflatoxin B1 and Aflatoxicol by several fungi. Appl. Environ. Microbiol. 1990, 56, 1465–1470. [Google Scholar] [CrossRef] [Green Version]
- Raney, K.D.; Gopalakrishnan, S.; Byrd, S.; Stone, M.P.; Harris, T.M. Alteration of the aflatoxin cyclopentenone ring to a delta-lactone reduces intercalation with DNA and decreases formation of guanine N7 adducts by aflatoxin epoxides. Chem. Res. Toxicol. 1990, 3, 254–261. [Google Scholar] [CrossRef] [PubMed]
- Kobertz, W.R.; Wang, D.; Wogan, G.N.; Essigmann, J.M. An intercalation inhibitor altering the target selectivity of DNA damaging agents: Synthesis of site-specific aflatoxin B1 adducts in a p53 mutational hotspot. Proc. Natl. Acad. Sci. USA 1997, 94, 9579–9584. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gopalakrishnan, S.; Harris, T.M.; Stone, M.P. Intercalation of aflatoxin B1 in two oligodeoxynucleotide adducts: Comparative 1H NMR analysis of d(ATCAFBGAT). d(ATCGAT) and d(ATAFBGCAT)2. Biochemistry 1990, 29, 10438–10448. [Google Scholar] [CrossRef] [PubMed]
- Smela, M.E.; Hamm, M.L.; Henderson, P.T.; Harris, C.M.; Harris, T.M.; Essigmann, J.M. The aflatoxin B(1) formamidopyrimidine adduct plays a major role in causing the types of mutations observed in human hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 2002, 99, 6655–6660. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lin, Y.C.; Li, L.; Makarova, A.V.; Burgers, P.M.; Stone, M.P.; Lloyd, R.S. Error-prone replication bypass of the primary aflatoxin B1 DNA adduct, AFB1-N7-Gua. J. Biol. Chem. 2014, 289, 18497–18506. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Levin, D.E.; Hollstein, M.; Christman, M.F.; Schwiers, E.A.; Ames, B.N. A new Salmonella tester strain (TA102) with A X T base pairs at the site of mutation detects oxidative mutagens. Proc. Natl. Acad. Sci. USA 1982, 79, 7445–7449. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shen, H.M.; Shi, C.Y.; Shen, Y.; Ong, C.N. Detection of elevated reactive oxygen species level in cultured rat hepatocytes treated with aflatoxin B1. Free Radic. Biol. Med. 1996, 21, 139–146. [Google Scholar] [CrossRef]
- Liu, J.; Yang, C.F.; Lee, B.L.; Shen, H.M.; Ang, S.G.; Ong, C.N. Effect of Salvia miltiorrhiza on aflatoxin B1-induced oxidative stress in cultured rat hepatocytes. Free Radic. Res. 1999, 31, 559–568. [Google Scholar] [CrossRef]
- Liu, Y.; Wang, W. Aflatoxin B1 impairs mitochondrial functions, activates ROS generation, induces apoptosis and involves Nrf2 signal pathway in primary broiler hepatocytes. Anim. Sci. J. 2016, 87, 1490–1500. [Google Scholar] [CrossRef]
- Li, H.; Zhang, L.X.; Wang, J.; Zheng, N. The Toxic Effects of Aflatoxin B1 and Aflatoxin M1 on Kidney through Regulating L-Proline and Downstream Apoptosis. Biomed. Res. Int. 2018, 12, 9074861. [Google Scholar] [CrossRef] [Green Version]
- Gesing, A.; Karbownik-Lewinska, M. Protective effects of melatonin and N-acetylserotonin on aflatoxin B1-induced lipid peroxidation in rats. Cell Biochem. Funct. 2008, 26, 314–319. [Google Scholar] [CrossRef] [PubMed]
- Theumer, M.G.; Cánepa, M.C.; López, A.G.; Mary, V.S.; Dambolena, J.S.; Rubinstein, H.R. Subchronic mycotoxicoses in Wistar rats: Assessment of the in vivo and in vitro genotoxicity induced by fumonisins and aflatoxin B1, and oxidative stress biomarkers status. Toxicology 2010, 268, 104–110. [Google Scholar] [CrossRef]
- Guindon, K.A.; Bedard, L.L.; Massey, T.E. Elevation of 8-hydroxydeoxyguanosine in DNA from isolated mouse lung cells following in vivo treatment with aflatoxin B1. Toxicol. Sci. 2007, 98, 57–62. [Google Scholar] [CrossRef] [Green Version]
- Coskun, E.; Jaruga, P.; Vartanian, V.; Erdem, O.; Egner, P.A.; Groopman, J.D.; Lloyd, R.S.; Dizdaroglu, M. Aflatoxin-Guanine DNA Adducts and Oxidatively Induced DNA Damage in Aflatoxin-Treated Mice in Vivo as Measured by Liquid Chromatography-Tandem Mass Spectrometry with Isotope Dilution. Chem. Res. Toxicol. 2019, 32, 80–89. [Google Scholar] [CrossRef] [PubMed]
- Kouvelis, V.N.; Wang, C.; Skrobek, A.; Pappas, K.M.; Typas, M.A.; Butt, T.M. Assessing the cytotoxic and mutagenic effects of secondary metabolites produced by several fungal biological control agents with the Ames assay and the VITOTOX® test. Mutat. Res. 2011, 722, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Said, B.; Ross, M.K.; Hamade, A.K.; Matsumoto, D.C.; Shank, R.C. DNA-damaging effects of genotoxins in mixture: Non additive effects of aflatoxin B1 and N-acetylaminofluorene on their mutagenicity in Salmonella typhimurium. Toxicol. Sci. 1999, 52, 226–231. [Google Scholar] [CrossRef] [PubMed]
- McKean, C.; Tang, L.; Tang, M.; Billam, M.; Wang, Z.; Theodorakis, C.W.; Kendall, R.J.; Wang, J.S. Comparative acute and combinative toxicity of aflatoxin B1 and fumonisin B1 in animals and human cells. Food Chem. Toxicol. 2006, 44, 868–876. [Google Scholar] [CrossRef]
- Theumer, M.G.; López, A.G.; Aoki, M.P.; Cánepa, M.C.; Rubinstein, H.R. Subchronic mycotoxicoses in rats. Histopathological changes and modulation of the sphinganine to sphingosine (Sa/So) ratio imbalance induced by Fusarium verticillioides culture material, due to the coexistence of aflatoxin B1 in the diet. Food Chem. Toxicol. 2008, 46, 967–977. [Google Scholar] [CrossRef]
- Golli-Bennour, E.E.; Kouidhi, B.; Bouslimi, A.; Abid-Essefi, S.; Hassen, W.; Bacha, H. Cytotoxicity and genotoxicity induced by aflatoxin B1, ochratoxin A, and their combination in cultured Vero cells. J. Biochem. Mol. Toxicol. 2010, 24, 42–50. [Google Scholar]
- Kim, J.; Park, S.H.; Do, K.H.; Kim, D.; Moon, Y. Interference with mutagenic aflatoxin B1-induced checkpoints through antagonistic action of ochratoxin A in intestinal cancer cells: A molecular explanation on potential risk of crosstalk between carcinogens. Oncotarget 2016, 7, 39627–39639. [Google Scholar] [CrossRef] [Green Version]
- Garon, D.; El Kaddoumi, A.; Carayon, A.; Amiel, C. FT-IR spectroscopy for rapid differentiation of Aspergillus flavus, Aspergillus fumigatus, Aspergillus parasiticus and characterization of aflatoxigenic isolates collected from agricultural environment. Mycopathologia 2010, 170, 131–142. [Google Scholar] [CrossRef]
- Samson, R.A.; Visagie, C.M.; Houbraken, J.; Hong, S.B.; Hubka, V.; Klaassen, C.H.W.; Perrone, G.; Seifert, K.A.; Susca, A.; Tanney, J.B.; et al. Phylogeny, identification and nomenclature of the genus Aspergillus. Stud. Mycol. 2014, 78, 141–173. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pottier, D.; André, V.; Rioult, J.P.; Bourreau, A.; Duhamel, C.; Kientz-Bouchart, V.; Richard, E.; Guibert, M.; Vérité, P.; Garon, D. Airborne molds and mycotoxins in Serpula lacrymans–damaged homes. Atmos. Pollut. Res. 2014, 5, 325–334. [Google Scholar] [CrossRef] [Green Version]
- Maron, D.M.; Ames, B.N. Revised methods for the Salmonella mutagenicity test. Mutat. Res. 1983, 113, 173–215. [Google Scholar] [CrossRef]
- André, V.; Lebailly, P.; Pottier, D.; Deslandes, E.; De Méo, M.; Henry-Amar, M.; Gauduchon, P. Urine mutagenicity of farmers occupationally exposed during a 1-day use of chlorothalonil and insecticides. Int. Arch. Occup. Environ. Health 2003, 76, 55–62. [Google Scholar] [CrossRef] [PubMed]
Extracts | Mycotoxins (µg/g Plug) | ||
---|---|---|---|
AFB1 | AFB2 | AFM1 | |
(Flav +) | 12.14 | 0.23 | 0.20 |
(Flav −) | <QL | <QL | <QL |
(Para +) | 0.30 | 0.006 | <QL |
(Para −) | <QL | <QL | <QL |
GLIO | VER | FUM | |
(FumiGlio+) | 11.6 | 0.04 | 0.23 |
(FumiGlio−) | <QL | 0.07 | 0.13 |
Extract Type | Mycotoxins (µg/Plate) | Mutagenicity (−S9 mix) (Rev/Plate a) | |||||||
---|---|---|---|---|---|---|---|---|---|
AFB1 | AFB2 | AFM1 | Whole Extract | AFB1+AFB2 | AFB1+AFM1 | AFB2+AFM1 | AFB1+AFB2+AFM1 | ||
(Flav−) | <QL | <QL | <QL | TA98–S9 SRN = 26 ± 10 | 17 ± 4 | - | - | - | |
(Flav+) | 0.7500 | 0.0140 | 0.0130 | 362 ± 25 | 73 ± 7 | 61 ± 7 | 12 ± 5 | 76 ± 9 | |
0.3000 | 0.0056 | 0.0052 | 106 ± 6 | 45 ± 6 | 45 ± 5 | 16 ± 9 | 48 ± 10 | ||
0.1500 | 0.0028 | 0.0026 | 41 ± 8 | 33 ± 7 | 42 ± 4 | 18 ± 12 | 41 ± 15 | ||
(Flav−) | <QL | <QL | <QL | TA100–S9 SRN = 146 ± 32 | 105 ± 12 | - | - | - | - |
(Flav+) | 0.5000 | 0.0093 | 0.0087 | 1031 ± 178 | 240 ± 33 | 231 ± 56 | 127 ± 14 | 184 ± 23 | |
0.3000 | 0.0056 | 0.0052 | 685 ± 28 | 222 ± 21 | 181 ± 49 | 144 ± 13 | 205 ± 39 | ||
0.1500 | 0.0028 | 0.0026 | 344 ± 35 | 190 ± 31 | 154 ± 29 | 151 ± 23 | 140 ± 23 | ||
(Flav−) | <QL | <QL | <QL | TA102–S9 SRN = 485 ± 63 | 427 ± 40 | - | - | - | - |
(Flav+) | 0.7500 | 0.0140 | 0.0130 | 446 ± 10 | 507 ± 37 | 492 ± 61 | 490 ± 57 | 509 ± 32 | |
0.5000 | 0.0093 | 0.0087 | 475 ± 41 | 473 ± 39 | 471 ± 46 | 462 ± 73 | 458 ± 108 | ||
0.1500 | 0.0028 | 0.0026 | 490 ± 25 | 511 ± 49 | 478 ± 55 | 444 ± 63 | 502 ± 37 |
Extract Type | Mycotoxins (µg/Plate) | Mutagenicity (+S9mix) (Rev/Plate a) | |||||||
---|---|---|---|---|---|---|---|---|---|
AFB1 | AFB2 | AFM1 | Whole Extract | AFB1+AFB2 | AFB1+AFM1 | AFB2+AFM1 | AFB1+AFB2+AFM1 | ||
(Flav−) | <QL | <QL | <QL | TA98 + S9 SRN = 27 ± 10 | 28 ± 6 | - | - | - | - |
(Flav+) | 0.0750 | 0.0014 | 0.0013 | 2154 ± 111 | 603 ± 83 | 413 ± 71 | 20 ± 13 | 200 ± 38 | |
0.0250 | 0.0005 | 0.0004 | 1183 ± 61 | 248 ± 72 | 123 ± 14 | 22 ± 8 | 50 ± 3 | ||
0.0050 | 0.0001 | 0.0001 | 183 ± 26 | 53 ± 8 | 47 ± 5 | 21 ± 11 | 63 ± 34 | ||
(Flav−) | <QL | <QL | <QL | TA100 + S9 SRN = 156 ± 43 | 105 ± 25 | - | - | - | - |
(Flav+) | 0.0250 | 0.0005 | 0.0004 | 1905 ± 39 | 635 ± 56 | 783 ± 55 | 153 ± 39 | 306 ± 51 | |
0.0050 | 0.0001 | 0.0001 | 861 ± 84 | 253 ± 23 | 265 ± 12 | 152 ± 14 | 136 ± 61 | ||
0.0010 | 0.00002 | 0.00002 | 227 ± 36 | nd | nd | nd | 185 ± 22 | ||
(Flav−) | <QL | <QL | <QL | TA102 + S9 SRN = 480 ± 65 | 409 ± 11 | - | - | - | - |
(Flav+) | 0.5000 | 0.0100 | 0.0080 | 2222 ± 75 | 539 ± 67 | 467 ± 78 | 481 ± 71 | 500 ± 26 | |
0.3000 | 0.0030 | 0.0048 | 1699 ± 69 | 529 ± 56 | 497 ± 40 | 475 ± 87 | 493 ± 23 | ||
0.1500 | 0.0015 | 0.0024 | 806 ± 41 | 578 ± 130 | 458 ± 29 | 488 ± 132 | 502 ± 67 |
Extract Type | Mycotoxins (µg/Plate) | Mutagenicity (−S9mix) (Rev/Plate a) | |||
---|---|---|---|---|---|
AFB1 | AFB2 | Whole Extract | AFB1+AFB2 | ||
(Para−) | <QL | <QL | TA98 – S9 SRN = 26 ± 10 | 27 ± 4 | - |
(Para+) | 0.3000 | 0.0050 | 249 ± 17 | 76 ± 9 | |
0.1500 | 0.0025 | 213 ± 16 | 48 ± 10 | ||
0.0500 | 0.0008 | 68 ± 20 | 41 ± 15 | ||
(Para−) | <QL | <QL | TA100 – S9 SRN = 146 ± 32 | 116 ± 7 | - |
(Para+) | 0.3000 | 0.0050 | 149 ± 19 | 184 ± 23 | |
0.1500 | 0.0025 | 167 ± 24 | 205 ± 39 | ||
0.0500 | 0.0008 | 139 ± 4 | 140 ± 23 | ||
(Para−) | <QL | <QL | TA102 – S9 SRN = 485 ± 63 | 372 ± 22 | - |
(Para+) | 0.3000 | 0.0050 | 470 ± 22 | 509 ± 32 | |
0.1500 | 0.0025 | 475 ± 19 | 458 ± 108 | ||
0.0500 | 0.0008 | 450 ± 26 | 502 ± 37 |
Extract Type | Mycotoxins (µg/Plate) | Mutagenicity (+S9mix) (Rev/Plate a) | |||
---|---|---|---|---|---|
AFB1 | AFB2 | Whole Extract | AFB1+AFB2 | ||
(Para−) | <QL | <QL | TA98 + S9 SRN = 26 ± 10 | 23 ± 1 | - |
(Para+) | 0.0050 | 0.0001 | 358 ± 36 | 125 ± 40 | |
0.0025 | 0.00005 | 141 ± 19 | 57 ± 8 | ||
0.0010 | 0.00002 | 60 ± 1 | 29 ± 2 | ||
(Para−) | <QL | <QL | TA100 + S9 SRN = 146 ± 32 | 126 ± 15 | - |
(Para+) | 0.0050 | 0.0001 | 487 ± 27 | 232 ± 8 | |
0.0025 | 0.00005 | 247 ± 14 | 187 ± 8 | ||
0.0010 | 0.00002 | 160 ± 19 | 142 ± 27 | ||
(Para−) | <QL | <QL | TA102 + S9 SRN =4 80 ± 65 | 446 ± 20 | - |
(Para+) | 0.3000 | 0.0050 | 751 ± 38 | 759 ± 36 | |
0.1500 | 0.0025 | 664 ± 63 | 579 ± 21 | ||
0.0500 | 0.0008 | 528 ± 4 | 489 ± 23 |
Extract Type | [Mycotoxins] (µg/Plate) | Mutagenicity (−S9mix) (Rev/Plate a) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
GLIO | FUM | VER | Whole Extract | FUM+VER ± GLIO | |||||||
(FumiGlio+) | 2.050 | 0.040 | 0.010 | TA98 – S9 SRN = 20 ± 3 | 22 | ± | 8 | 22 | ± | 7 | |
0.410 | 0.008 | 0.002 | 18 | ± | 4 | 23 | ± | 2 | |||
(FumiGlio−) | <QL | 0.0130 | 0.0240 | 17 | ± | 4 | 26 | ± | 7 | ||
<QL | 0.0026 | 0.0048 | 19 | ± | 1 | 24 | ± | 1 | |||
(FumiGlio+) | 2.050 | 0.040 | 0.010 | TA100 – S9 SRN=122 ± 22 | 179 | ± | 44 | 141 | ± | 6 | |
0.410 | 0.008 | 0.002 | 142 | ± | 6 | 141 | ± | 7 | |||
(FumiGlio−) | <QL | 0.0130 | 0.0240 | 123 | ± | 9 | 119 | ± | 5 | ||
<QL | 0.0026 | 0.0048 | 147 | ± | 17 | 125 | ± | 25 | |||
(FumiGlio+) | 2.050 | 0.040 | 0.010 | TA102 – S9 SRN = 424 ± 13 | 494 | ± | 137 | 432 | ± | 48 | |
0.410 | 0.008 | 0.002 | 443 | ± | 37 | 423 | ± | 45 | |||
(FumiGlio−) | <QL | 0.0130 | 0.0240 | 462 | ± | 23 | 403 | ± | 40 | ||
<QL | 0.0026 | 0.0048 | 395 | ± | 16 | 417 | ± | 15 |
Extract Type | [Mycotoxins] (µg/Plate) | Mutagenicity (Rev/Plate a) | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
GLIO | FUM | VER | Whole Extract | FUM+VER±GLIO | ||||||
(FumiGlio+) | 2.050 | 0.040 | 0.010 | TA98 + S9 SRN = 19 ± 2 | 23 | ± | 1 | 22 | ± | 1 |
0.410 | 0.008 | 0.002 | 21 | ± | 7 | 22 | ± | 2 | ||
(FumiGlio−) | <QL | 0.0130 | 0.0240 | 18 | ± | 1 | 22 | ± | 1 | |
<QL | 0.0026 | 0.0048 | 16 | ± | 5 | 22 | ± | 2 | ||
(FumiGlio+) | 2,050 | 0.040 | 0.010 | TA100 + S9 SRN = 92 ± 23 | 103 | ± | 9 | 116 | ± | 18 |
0,410 | 0.008 | 0.002 | 73 | ± | 5 | 122 | ± | 9 | ||
(FumiGlio−) | <QL | 0.0130 | 0.0240 | 123 | ± | 21 | 117 | ± | 10 | |
<QL | 0.0026 | 0.0048 | 95 | ± | 16 | 130 | ± | 8 | ||
(FumiGlio+) | 2.050 | 0.040 | 0.010 | TA102 + S9 SRN = 388 ± 28 | 539 | ± | 37 | 373 | ± | 29 |
0.410 | 0.008 | 0.002 | 442 | ± | 3 | 395 | ± | 24 | ||
(FumiGlio−) | <QL | 0.0130 | 0.0240 | 516 | ± | 34 | 393 | ± | 11 | |
<QL | 0.0026 | 0.0048 | 392 | ± | 22 | 361 | ± | 54 |
Mycotoxins | Concentration (µg/Plate) | Mutagenicity (Revertants/Plate a) | |||
---|---|---|---|---|---|
TA98 | TA100 | TA102 | |||
None | −S9 +S9 | 0 0 | 26 ± 10 27 ± 10 | 146 ± 32 156 ± 43 | 485 ± 63 480 ± 65 |
AFB1 | −S9 | 0.7500 0.5000 0.3000 0.1500 | 106 ± 40 nd 53 ± 14 29 ± 10 | nd 272 ± 95 201 ± 48 154 ± 35 | 419 ± 86 458 ± 73 nd 472 ± 91 |
+S9 | 0,5000 0.3000 0.1500 0.0750 0.0250 0.0050 0.0010 | nd nd (T) 1075 ± 112 275 ± 20 88 ± 13 nd | nd nd nd (T) 1050 ± 161 279 ± 37 139 ± 38 | 473 ± 112 482 ± 133 501 ± 104 nd nd nd nd | |
AFB2 | −S9 | 0.0140 0.0050 0.0010 | 20 ± 3 20 ± 2 20 ± 2 | 132 ± 7 128 ± 6 127 ± 17 | 461 ± 14 476 ± 27 449 ± 26 |
+S9 | 0.0140 0.0050 0.0010 | 28 ± 4 25 ± 6 23 ± 1 | 142 ± 12 157 ± 9 127 ± 2 | 416 ± 18 418 ± 22 429 ± 17 | |
AFM1 | −S9 | 0.0130 0.0020 | 18 ± 2 18 ± 3 | 186 ± 2 183 ± 10 | 461 ± 14 463 ± 45 |
+S9 | 0.0013 0.0002 | 23 ± 4 32 ± 2 | 161 ± 11 168 ± 6 | 475 ± 45 439 ± 27 | |
FUM | −S9 | 0.0400 0.0250 0.0090 | 18 ± 2 19 ± 2 22 ± 1 | 140 ± 10 149 ± 6 148 ± 9 | 468 ± 34 451 ± 38 439 ± 6 |
+S9 | 0.0400 0.0250 0.0090 | 30 ± 11 28 ± 2 31 ± 1 | 133 ± 3 123 ± 19 127 ± 2 | 460 ± 7 485 ± 30 493 ± 17 | |
GLIO | −S9 | 2.0500 0.4100 | 17 ± 4 20 ± 4 | 130 ± 8 131 ± 1 | 457 ± 18 454 ± 20 |
+S9 | 2.0500 0.4100 | 20 ± 1 22 ± 1 | 148 ± 8 148 ± 7 | 414 ± 17 388 ± 21 | |
VER | −S9 | 0.0100 0.0050 | 17 ± 2 19 ± 1 | 141 ± 12 145 ± 10 | 442 ± 30 467 ± 19 |
+S9 | 0.0100 0.0050 | 28 ± 3 28 ± 5 | 157 ± 6 158 ± 13 | 494 ± 8 349 ± 12 |
Strains | S9 | Revertants/ngAFB1 | ||
---|---|---|---|---|
Extracts | Pure AFB1 | |||
(Flav+) | (Para+) | |||
TA98 | − | 0.5 | 1.4 | 0.18 |
+ | 47.3 | 71.6 | 17.6 | |
TA100 | − | 2.3 | - | 0.5 |
+ | 172.2 | 99 | 55.8 | |
TA102 | − | - | - | - |
+ | 5.7 | 4.4 | - |
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Lanier, C.; Garon, D.; Heutte, N.; Kientz, V.; André, V. Comparative Toxigenicity and Associated Mutagenicity of Aspergillus fumigatus and Aspergillus flavus Group Isolates Collected from the Agricultural Environment. Toxins 2020, 12, 458. https://doi.org/10.3390/toxins12070458
Lanier C, Garon D, Heutte N, Kientz V, André V. Comparative Toxigenicity and Associated Mutagenicity of Aspergillus fumigatus and Aspergillus flavus Group Isolates Collected from the Agricultural Environment. Toxins. 2020; 12(7):458. https://doi.org/10.3390/toxins12070458
Chicago/Turabian StyleLanier, Caroline, David Garon, Natacha Heutte, Valérie Kientz, and Véronique André. 2020. "Comparative Toxigenicity and Associated Mutagenicity of Aspergillus fumigatus and Aspergillus flavus Group Isolates Collected from the Agricultural Environment" Toxins 12, no. 7: 458. https://doi.org/10.3390/toxins12070458