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Published Version DISS. ETH Nr. 27188 Detection of aquatic wildlife pathogens from eDNA in water samples Validation and Application in Switzerland A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zürich) presented by NATALIE MARIETTA SIEBER Master of Science ETH in Environmental Sciences born on 15.03.1991 citizen of Zurich, Switzerland accepted on the recommendation of Prof. Dr. Christoph Vorburger Dr. Hanna Hartikainen Dr. Armin Zenker Prof. Dr. Jukka Jokela Dr. Trude Vrålstad 2020 Table of Contents Summary 3 Zusammenfassung 5 General Introduction 7 Chapter 1 35 Validation of an eDNA-based method for the detection of wildlife pathogens in water Chapter 2 77 Parasite DNA detection in water samples enhances crayfish plague (Aphanomyces astaci) monitoring in asymptomatic carrier populations Chapter 3 111 A survey of multiple aquatic wildlife pathogens of concern in Switzerland using an eDNA-based method for detection in water Chapter 4 159 Synthesis: remaining challenges and opportunities Acknowledgements 175 2 Summary Emergent diseases are contributing to the decline of various freshwater species already facing multiple threats of anthropogenic origin, such as habitat degradation, climate change and species introductions. One of the most ecologically important diseases is the crayfish plague, caused by the oomycete Aphanomyces astaci, responsible for widespread population collapses of native European freshwater crayfish species. The chytrid fungus Batrachochytrium dendrobatidis is another highly problematic pathogen and major contributor of amphibian declines worldwide, its spread being promoted by animal trade. Saprolegnia parasitica, closely related to A. astaci and causal agent of Saprolegniosis, widely occurs in freshwater habitats and can cause high mortality outbreaks in fish. Proliferative kidney disease (PKD), caused by the myxozoan Tetracapsuloides bryosalmonae, severely impacts wild salmonid stocks and trout farms. Due to its temperature-dependent development, climate change is expected to increase the disease’s impact on host populations. Mitigation and prevention of negative impacts caused by emergent diseases is of interest for species conservation and from an economic viewpoint. Therefore, effective management measures need to be devised, which in turn, require close and comprehensive surveillance of diseases and their agents. However, regularity and scope of monitoring campaigns are often impeded by the high costs and effort required for conventional disease monitoring methods, which often focus on the capture and examination of host species. Furthermore, such methods are usually limited to host species of the same taxonomic groups, such as fish or amphibians. DNA acquired from the target organism’s environment (e.g. water or soil) and not directly from the target itself, is called environmental DNA (eDNA). Using eDNA-based techniques, waterborne pathogens can be directly detected in water, omitting the need for laborious host capture, which renders them less cost- and time-intensive than conventional detection methods. Also, eDNA-based detection is more adaptable to detection of multiple pathogen species across taxonomic boundaries, since they are not limited to single host taxonomic groups. Therefore, eDNA-based methods could facilitate more regular and comprehensive disease monitoring campaigns. The central aim of this thesis was to develop, test and apply an eDNA-based method and workflow for the detection of aquatic wildlife pathogens in water. More specifically, the four 3 Summary species presented above, A. astaci, B. dendrobatidis, S. parasitica and T. bryosalmonae and their detection in water, using already published quantitative real-time PCR assays, was analysed. In a controlled environment I tested the effect of water source and estimated zoospore concentrations on the reliability of B. dendrobatidis and T. bryosalmonae detection in water (Chapter 1). Detection consistency was surprisingly low for both pathogens, though even low estimated zoospore concentrations were detected. Likely reasons for the observed imperfect detection of the two pathogens could have been the heterogeneous distribution of zoospores in the water and variability in DNA extraction efficiency introduced by the filter. The performance of the developed method for detecting A. astaci in water was compared to detection of the pathogen in crayfish tissue from individuals collected from the same sampling sites (Chapter 2). Results of the two methods only partly overlapped, indicating that reliable detection in asymptomatic carrier populations is challenging. A combination of both water and tissue sampling methods for surveillance could therefore create a more accurate picture of A. astaci occurrence. In a country-wide survey, water samples were collected and analysed for the four pathogens A. astaci, B. dendobatidis, S. parasitica and T. bryosalmonae, applying the eDNA-based method I developed (Chapter 3). Widespread distribution of A. astaci, S. parasitica and T. bryosalmonae in water samples was found, reflecting prior surveys and expectations. Rare detection of B. dendrobatidis was likely due to inappropriate site selection for amphibians. This survey showed the feasibility of monitoring multiple pathogens using eDNA-based techniques, albeit limitations are still imposed by pathogen and host properties, such as habitat range. In a concluding chapter, I discuss implications of the results of the previous chapters and propose ways for improvement. I further discuss areas of research and topics I deem important for the future development and application of eDNA-based methods for disease surveillance. 4 Zusammenfassung Viele Süsswasserarten werden, nebst anthropogenen Beeinflussungen, wie Verschlechterung des Lebensraumes, Klimawandel und invasive Arteinführungen, durch neuaufkommende Krankheiten bedroht. Eine der gefährlichsten Krankheiten ist die Krebspest, welche vom Eipilz Aphanomyces astaci verursacht wird und den Kollaps vieler europäischer Flusskrebspopulationen herbeigeführt hat. Der Chytridpilz Batrachochytrium dendrobatidis ist ein weiterer problematischer Krankheitserreger, deren Verbreitung durch den internationalen Tierhandel begünstigt wird und mitverantwortlich ist für Rückgänge von Amphibienpopulationen weltweit. Die mit A. astaci nah verwandte Saprolegnia parasitica, Verursacherin von Saprolegniose, kommt in fast allen Süsswassergewässern vor und kann hohe Mortalitäten in Fischbeständen verursachen. Die Proliferative Nierenkrankheit (PKD), mit dem Myxozoten Tetracapsuloides bryosalmonae als Erreger, hat grosse negative Auswirkungen auf sowohl wilde Salmonide als auch in Fischzuchten. Durch ihre temperaturbedingte Entwicklung wird eine weitere Ausbreitung durch die Klimaerwärmung erwartet. Die Eindämmung und Präventation von negativen Auswirkungen durch aquatische Krankheiten ist wichtig für den Artenschutz. Hierfür müssen effektive Massnahmen geplant und umgesetzt werden, was nur mit ausführlichem Wissen über das Vorkommen der Krankheitserreger möglich ist. Die Umsetzung von umfassenden Monitorings von solchen Krankheiten wird oft durch hohe Kosten und Aufwand erschwert. Konventionelle Methoden beinhalten meist das Einfangen von Wirtsindividuen und deren Untersuchung im Labor. Oft sind sie deswegen auch auf eine einzelne taxonomische Einheit von Wirtsarten beschränkt, z.B. Fische oder Amphibien. DNA, welche der Umwelt des Zielorganismus (z.B. Wasser oder Boden) und nicht direkt dem Organismus, entzogen wird, nennt sich Umwelt-DNA (engl. eDNA). Auf eDNA basierende Methoden können Krankheitserreger direkt im Wasser nachweisen, ohne den Wirt suchen zu müssen und sind daher mit weniger Aufwand und Kosten verbunden als konventionelle Methoden. Zudem ist die Umwelt-DNA Methode flexibler beim Nachweis mehrerer Erregerarten aus verschiedenen taxonomischen Gruppen, weil sie weniger an eine Wirtsart gebunden ist. Umwelt-DNA Methoden könnten aus diesen Gründen die regelmässige und umfassende Überwachung von Krankheiten erleichtern. 5 Zusammenfassung Das Hauptziel dieser Arbeit war die Entwicklung, das Testen und Anwenden einer Umwelt- DNA Methode für den Nachweis von Krankheitserreger aquatischer Wildtiere in Wasser. Die vier erwähnten Erreger, A. astaci, B. dendrobatidis, S. parasitica und T. bryosalmonae und deren Nachweis in Wasser mithilfe bereits veröffentlichter quantitative real-time PCR Untersuchungen, wurden analysiert. In kontrollierter Umgebung habe ich den Effekt von Wasserherkunft und geschätzter Zoosporenkonzentrationen auf die Nachweiszuverlässigkeit von B. dendrobatidis und T. bryosalmonae in Wasser getestet (Kapitel 1). Beide Erreger konnten nur unregelmässig in Wasserproben nachgewiesen werden. Dieses Muster könnte durch die ungleichmässige Verteilung der Sporen im Wasser und der Effizienzvariabilität der DNA Extraktion durch den Filter, verursacht werden. Die in dieser Arbeit entwickelte Umwelt-DNA Methode wurde zudem mit einer konventionellen Methode für den Nachweis von A. astaci verglichen (Kapitel 2). Hierfür wurden sowohl Wasser- als auch Gewebeproben von Flusskrebsen am selben Standort analysiert. Die Resultate beider Methoden stimmten nur teilweise überein, was verdeutlicht, wie schwierig der verlässliche Nachweis des Erregers in asymptomatischen Wirtspopulationen ist. Eine Kombination beider Methoden für die Überwachung des Krankheitserregers könnte ein genaueres Bild der Verbreitung von A. astaci schaffen. Die Verbreitung der vier Krankheitserreger A. astaci, B. dendobatidis,
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