Chemotaxonomy of Mycotoxigenic Small-Spored Fungi - Do Multitoxin Mixtures Act As an Indicator for Species Differentiation?

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2018 Jul 19

PMID 30018598

Citations 16

Authors

Theresa Zwickel

Sandra M Kahl

Michael Rychlik

Marina E H Muller

Affiliations

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Abstract

Necrotrophic as well as saprophytic small-spored species are annually responsible for major losses of agricultural products, such as cereal crops, associated with the contamination of food and feedstuff with potential health-endangering toxins. Knowledge of the metabolic capabilities of different species-groups to form mycotoxins is of importance for a reliable risk assessment. 93 strains belonging to the four species groups , , , and were isolated from winter wheat kernels harvested from fields in Germany and Russia and incubated under equal conditions. Chemical analysis by means of an HPLC-MS/MS multi--toxin-method showed that 95% of all strains were able to form at least one of the targeted 17 non-host specific toxins. Simultaneous production of up to 15 (modified) toxins by members of the , , species-groups and up to seven toxins by strains was demonstrated. Overall tenuazonic acid was the most extensively formed mycotoxin followed by alternariol and alternariol mono methylether, whereas altertoxin I was the most frequently detected toxin. Sulfoconjugated modifications of alternariol, alternariol mono methylether, altenuisol and altenuene were frequently determined. Unknown perylene quinone derivatives were additionally detected. Strains of the species-group could be segregated from strains of the other three species-groups due to significantly lower toxin levels and the specific production of infectopyrone. Apart from infectopyrone, alterperylenol was also frequently produced by 95% of the strains. Neither by the concentration nor by the composition of the targeted toxins a differentiation between the species-groups , and was possible.

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References

Lee H, Patriarca A, Magan N . Alternaria in Food: Ecophysiology, Mycotoxin Production and Toxicology. Mycobiology. 2015; 43(2):93-106. PMC: 4505009. DOI: 10.5941/MYCO.2015.43.2.93. View

Schaberle T . Biosynthesis of α-pyrones. Beilstein J Org Chem. 2016; 12:571-88. PMC: 4901931. DOI: 10.3762/bjoc.12.56. View

Schwarz C, Tiessen C, Kreutzer M, Stark T, Hofmann T, Marko D . Characterization of a genotoxic impact compound in Alternaria alternata infested rice as Altertoxin II. Arch Toxicol. 2012; 86(12):1911-25. DOI: 10.1007/s00204-012-0958-4. View

da Cruz Cabral L, Rodriguero M, Stenglein S, Nielsen K, Patriarca A . Characterization of small-spored Alternaria from Argentinean crops through a polyphasic approach. Int J Food Microbiol. 2017; 257:206-215. DOI: 10.1016/j.ijfoodmicro.2017.06.026. View

Woudenberg J, Groenewald J, Binder M, Crous P . Alternaria redefined. Stud Mycol. 2013; 75(1):171-212. PMC: 3713888. DOI: 10.3114/sim0015. View

Zwickel T, Klaffke H, Richards K, Rychlik M . Development of a high performance liquid chromatography tandem mass spectrometry based analysis for the simultaneous quantification of various Alternaria toxins in wine, vegetable juices and fruit juices. J Chromatogr A. 2016; 1455:74-85. DOI: 10.1016/j.chroma.2016.04.066. View

Winter C, Gilchrist D, Dickman M, Jones C . Chemistry and biological activity of AAL toxins. Adv Exp Med Biol. 1996; 392:307-16. DOI: 10.1007/978-1-4899-1379-1_26. View

Vejdovszky K, Sack M, Jarolim K, Aichinger G, Somoza M, Marko D . In vitro combinatory effects of the Alternaria mycotoxins alternariol and altertoxin II and potentially involved miRNAs. Toxicol Lett. 2016; 267:45-52. DOI: 10.1016/j.toxlet.2016.12.011. View

Kahl S, Ulrich A, Kirichenko A, Muller M . Phenotypic and phylogenetic segregation of Alternaria infectoria from small-spored Alternaria species isolated from wheat in Germany and Russia. J Appl Microbiol. 2015; 119(6):1637-50. DOI: 10.1111/jam.12951. View

10.

Pero R, Posner H, Blois M, Harvan D, Spalding J . Toxicity of metabolites produced by the "Alternaria". Environ Health Perspect. 1973; 4:87-94. PMC: 1474843. DOI: 10.1289/ehp.730487. View

11.

Andersen B, Sorensen J, Nielsen K, Gerrits van den Ende B, de Hoog S . A polyphasic approach to the taxonomy of the Alternaria infectoria species-group. Fungal Genet Biol. 2009; 46(9):642-56. DOI: 10.1016/j.fgb.2009.05.005. View

12.

Frisvad J, Andersen B, Thrane U . The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycol Res. 2008; 112(Pt 2):231-40. DOI: 10.1016/j.mycres.2007.08.018. View

13.

Stack M, Mazzola E . Stemphyltoxin III from Alternaria alternata. J Nat Prod. 1989; 52(2):426-7. DOI: 10.1021/np50062a042. View

14.

Stewart J, Andrew M, Bao X, Chilvers M, Carris L, Peever T . Development of sequence characterized amplified genomic regions (SCAR) for fungal systematics: proof of principle using Alternaria, Ascochyta and Tilletia. Mycologia. 2013; 105(4):1077-86. DOI: 10.3852/12-287. View

15.

Woudenberg J, Seidl M, Groenewald J, de Vries M, Stielow J, Thomma B . Alternaria section Alternaria: Species, formae speciales or pathotypes?. Stud Mycol. 2016; 82:1-21. PMC: 4774270. DOI: 10.1016/j.simyco.2015.07.001. View

16.

Fleck S, Sauter F, Pfeiffer E, Metzler M, Hartwig A, Koberle B . DNA damage and repair kinetics of the Alternaria mycotoxins alternariol, altertoxin II and stemphyltoxin III in cultured cells. Mutat Res Genet Toxicol Environ Mutagen. 2016; 798-799:27-34. DOI: 10.1016/j.mrgentox.2016.02.001. View

17.

Vejdovszky K, Hahn K, Braun D, Warth B, Marko D . Synergistic estrogenic effects of Fusarium and Alternaria mycotoxins in vitro. Arch Toxicol. 2016; 91(3):1447-1460. PMC: 5316405. DOI: 10.1007/s00204-016-1795-7. View

18.

Lawrence D, Gannibal P, Peever T, Pryor B . The sections of Alternaria: formalizing species-group concepts. Mycologia. 2013; 105(3):530-46. DOI: 10.3852/12-249. View

19.

Klionsky D, Herman P, Emr S . The fungal vacuole: composition, function, and biogenesis. Microbiol Rev. 1990; 54(3):266-92. PMC: 372777. DOI: 10.1128/mr.54.3.266-292.1990. View

20.

Jarolim K, Del Favero G, Ellmer D, Stark T, Hofmann T, Sulyok M . Dual effectiveness of Alternaria but not Fusarium mycotoxins against human topoisomerase II and bacterial gyrase. Arch Toxicol. 2016; 91(4):2007-2016. PMC: 5364253. DOI: 10.1007/s00204-016-1855-z. View