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«Inauguraldissertation zur Erlangung der Würde eines Doktors der Philosophie vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der ...»

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Ecotoxicological characterization of the estrogenic

mycotoxin zearalenone and environmental samples:

Effects on zebrafish development and reproduction

Inauguraldissertation

zur

Erlangung der Würde eines Doktors der Philosophie

vorgelegt der

Philosophisch-Naturwissenschaftlichen Fakultät

der Universität Basel

von

Patrick Schwartz

aus Deutschland

Basel, 2011

 

 

Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät

auf Antrag von

Prof. Dr. Patricia Holm und Prof. Dr. Thomas Braunbeck Basel, den 14. Dezember 2010 Prof. Dr. Martin Spiess Dekan Originaldokument gespeichert auf dem Dokumentenserver der Universität Basel  edoc.unibas.ch        Dieses Werk ist unter dem Vertrag „Creative Commons Namensnennung‐Keine kommerzielle Nutzung‐ Keine Bearbeitung 2.5 Schweiz“ lizenziert. Die vollständige Lizenz kann unter   creativecommons.org/licences/by‐nc‐nd/2.5/ch  eingesehen werden.      Namensnennung-Keine kommerzielle Nutzung-Keine Bearbeitung 2.5 Schweiz

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–  –  –

Viele Menschen haben zum Gelingen dieser Arbeit beigetragen. Mein Dank dafür gilt:

Professor Dr. Patricia Holm für die Möglichkeit zu dieser Dissertation beim Programm MGU und Professor Dr. Thomas Braunbeck für die freundliche Übernahme des Korreferats;

Maria a Marca dafür, dass wir diesen oftmals nicht einfachen Weg zusammen gegangen sind und ihre Hilfsbereitschaft bei der Arbeit und darüber hinaus;

Nadja Häfeli für ihre sehr nette Gesellschaft, die unkomplizierte Zusammenarbeit und das Vertrauten dass sie mir entgegen brachte;

Katja Knauer dafür, dass sie mir nicht nur in der Welt der Naturwissenschaft jederzeit mit Rat und Tat zur Seite stand;

Sara Schubert, vor allem für ihre engagierte und einfühlsame Unterstützung aus dem fernen Osten und Oliver “El Doctor Gordito“ Körner, der immer ein offenes Ohr hatte und mich mit seinen reichen Erfahrungen unterstützte;

Karen Thorpe und Christian Michel für die fruchtbare Zusammenarbeit im Labor und auf dem Papier sowie ihre wertvollen Ratschläge und Ideen;

Thomas Bucheli für unser Mykotoxinprojekt und seine fachkundigen Beiträge sowie Felix Wettstein und Niccolo Hartmann für die gute Kooperation (Agroscope Reckenholz-Tänikon ART);

Karin Rüfenacht und Kerstin Dannenhauer für die überaus freundliche Unterstützung im Land der Molekularbiologie sowie Marc Suter und René Schönenberger für ihren grosszügigen Beitrag in der chemischen Analytik (EAWAG, Dübendorf);

Arno Stöckli und Michael Stampfli für die gute Kooperation, die Anregungen aus der Praxis und den Blick in die Unterwelt (Departement Bau, Verkehr und Umwelt, Aarau);

Heidi Schiffer, Lukas Zimmermann, Gabi Thoma, Marion Mertens, Catherine Fehlmann, Helge Abicht, Stefanie Knauert, Andrea Leimgruber, Felicitas Maeder, Barbara Collucci, Martha Grajales, Sophia Bloch, Tara Hadler, Nadia von Moos, Angela Solothurnmann, Nora Zuberbühler, Paul Burger, Heidi Arbogast, Alexandra Sauer, Yvonne Scherrer, Rainer Kamber, Wolfgang Zierhofer und Glaudio Gamboni für ihre freundliche Aufnahme, Hilfe und nette Gesellschaft.

–  –  –

The aquatic environment is particularly susceptible to pollution, partly because there is considerable intentional release of chemicals into rivers, lakes and the sea (mainly through release of effluents), and partly because it receives a lot of accidental releases of chemicals (through spills, runoff, atmospheric deposition, etc.). Sewage treatment plants (STPs) release a complex mixture of natural and synthetic chemicals into the aquatic environment. It was estimated that 60’000 man-made chemicals are in routine use worldwide, most of them enter the aquatic environment and many of them via STPs.





Endocrine disruption occurs when specific chemicals interact with internal endocrine signalling pathways in organisms. In the aquatic environment, endocrine active substances are easily bioavailable to fish through aquatic respiration, osmoregulation, maternal transfer into eggs, dermal contact with contaminated sediments or ingestion of contaminated food. Endocrine disruption appears to be particularly widespread in freshwater fish throughout the world. Effects ranged from subtle changes in the physiology and sexual behaviour of fish to permanently altered sexual differentiation and growth, and reproductive impairment. Most attention has been directed towards identifying the main estrogenic chemicals, because many of the effects reported in wildlife appear to be a consequence of ‘feminization’ of males. Environmental estrogens can be anthropogenic, such as certain pharmaceuticals, pesticides and industrial chemicals or natural, such as phyto- and mycoestrogens.

Resorcyclic acid lactones (RALs) are the only known class of estrogenic mycotoxins and show estrogenic activity in the range of natural steroid estrogens. RALs occur as secondary metabolites of Fusarium spec. fungi growing on a variety of cereals. Zearalenone (ZON) belongs to the chemical group of RALs and is one of the worldwide most common mycotoxins. The occurrence of mycotoxins has been studied extensively in food, feed products, and domestic animals. Agricultural products around the world exhibited ZON contaminations of up to 69 % of the tested samples. However, only little is known about the ecotoxicological effects of ZON at concentrations found in the environment. Only a few short-term in vivo studies investigated ZON and its metabolites and observed effects on vitellogenin (VTG) induction, zona radiata proteins, the immune system, and growth of fish after exposure via injection or feeding.

In this research project, the ecotoxicological potential of ZON was evaluated. Effects on fish caused by an exposure to ZON were assessed using the zebrafish (Danio rerio) as a model organism. An embryo toxicity test was performed to investigate toxic effects of ZON on fish development. This study was complemented with a 30 day zebrafish early life-stage experiment to assess the influence of ZON on juvenile growth. In a second step the estrogenic potency of

1   Summary

ZON and its effects on adult fish were examined. A recombinant yeast estrogen screen (rYES) was used as an in vitro assay to determine effects on the activation of estrogen receptor-regulated genes. Zebrafish were exposed to ZON in a 42 day reproduction experiment enabling assessment of reproductive as well as physiological and morphological parameters. In a third step, the estrogenic potency of ZON was studied in a life-cycle experiment. This study was designed to investigate possible effects of continuous long-term exposure including a subsequent depuration period as well as possible transgenerational effects of F0 exposure on F1 generation. The offspring of the F0 generation that was exposed to ZON for 21 days was raised in a 140 day exposure experiment from embryo to adult. In a subsequent 42 day reproduction experiment, spawning groups of the F1 generation were either exposed to ZON (after growing up in clean water) or clean water (after growing up under ZON exposure) and effects on developmental, reproductive as well as physiological parameters were assessed.

Exposure to ZON had no effects on embryonic development up to 2000 ng/L, but a positive correlation between the body length and ZON concentration of up to 100 ng/L suggests a growth promoting effect for zebrafish exposed during 30 days. Although ZON revealed a moderate estrogenic potency in vitro (rYES), it exhibited a comparably strong effect on induction of VTG (1000 ng/L) and reproduction (100 ng/L) in vivo during 21 days exposure. It was further demonstrated that ZON influenced growth (1000 ng/L), sexual differentiation (320 ng/L), reproduction (1000 ng/L), and VTG levels (1000 ng/L) in zebrafish exposed from fertilization to day 140. Furthermore, ZON revealed a possible transgenerational effect on growth caused by short-term exposure of F0 and F1 generation each for 21 days to 1000 ng/L.

In the framework of this project, relevant data of the ecotoxicological relevance of ZON were collected. The estrogenic potential of ZON was confirmed in vitro and in vivo and detrimental effects on zebrafish reproduction were demonstrated. This indicates that ZON may have an effect on fish populations in the aquatic environment. Effects were observed at concentrations near the maximum measured values in surface waters (approximately double) and below the maximum values measured in effluents (approximately half). Even though to date there is not much data published presenting ZON concentrations in the aquatic environment and effects on different (native) fish species, this project demonstrated that ZON has the potential to pose a threat to fish in the aquatic environment.

In a second research project, the embryo toxicity and genotoxicity of biofilm and sediment from the catchment area of a STP was investigated. An embryo toxicity test with zebrafish and the comet assay (single cell gel electrophoresis) with primary cells isolated from the embryos were applied to investigate native biofilm for the first time. Biofilms were sampled from different

2   Summary

sections of the sewage system and sediments were taken from the rive Wyna directly at, upstream and downstream of the STP discharge Mittleres Wynental (Switzerland). The aim of this study was to verify the applicability of the aforementioned test system to investigate native biofilm and to evaluate the toxicity of the different sampling sites.

Clear differences in the embryo toxicity and genotoxicity of the biofilm from different sewage system sections as well as from the sediment sampling sites were found. Significant genotoxicity was determined in all biofilm and sediment samples. Temporal variability in toxicity were observed in some of the biofilm and sediment samples. Based on the results of this study it can be suggested that biofilm implemented in ecotoxicological bioassays such as the embryo toxicity test and comet assay with zebrafish can be a useful tool to assess (waste) water quality.

–  –  –

1 Ecotoxicological characterization of the estrogenic mycotoxin zearalenone

1.1 The phenomenon: Endocrine disruption An endocrine disrupter has been defined as ‘an exogenous substance or mixture that alters function(s) of the endocrine system and consequently causes adverse effects in an intact organism, or its progeny, or subpopulations’ (Vos et al. 2000). Endocrine disruption occurs when exogenous chemicals interact with internal endocrine signalling pathways in an organism (Cheek et al. 1998). Endocrine active substances (EASs) may affect the development or reproduction of organisms by interfering with normal synthesis, storage, release, transport, metabolism, binding, action or elimination of endogenous hormones (Kavlock & Ankley 1996).

In general, the reproductive physiology of vertebrates, both mammalian and non-mammalian, is similar, with the broad structure and function of the reproductive axis involving the hypothalamus, pituitary and gonads conserved. In all vertebrates, the release of a decapeptide gonadotrophin-releasing hormone (GnRH) from the hypothalamus stimulates the pituitary to secrete gonadotrophic hormones (GTH) that signal the gonads to synthesize steroid hormones.

The basic biosynthetic pathways for steroid hormones and the active steroid hormones themselves are also well-conserved in both mammalian and non-mammalian vertebrates (Mills & Chichester 2005).

The aquatic environment is particularly susceptible to pollution, partly because there is considerable intentional release of chemicals into rivers, lakes and the sea (mainly through release of effluents from sewage treatment plants [STPs] and industries), and partly because it receives a lot of accidental releases of chemicals (through spills, runoff, atmospheric deposition, etc; Sumpter 2005). STPs (which often receive domestic, industrial and/or agricultural waste) release a complex mixture of natural and synthetic chemicals into the aquatic environment, following their partial or complete biodegradation during the treatment process. It is estimated that 60’000 man-made chemicals are in routine use worldwide and most of these enter the aquatic environment (Jobling & Tyler 2003).

Endocrine disruption appears to be particularly widespread in freshwater fish populations. There is little evidence, however, to suggest that fish are more susceptible to EASs relative to other



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