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Exemplary Investigations of Squirrels and Shrews As Relevant Virus

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Exemplary Investigations of Squirrels and Shrews As Relevant Virus Inaugural-Dissertation zur Erlangung der Doktorwürde der Tierärztlichen Fakultät der Ludwig-Maximilians-Universität München Exemplary investigations of squirrels and shrews as relevant virus reservoir hosts von Vanessa Schulze aus Essen München 2020 Aus dem Veterinärwissenschaftlichen Department der Tierärztlichen Fakultät der Ludwig-Maximilians-Universität München Lehrstuhl für Virologie Arbeit angefertigt unter der Leitung von Univ.-Prof. Dr. Gerd Sutter Angefertigt am Friedrich-Loeffler-Institut Insel Riems, Bundesforschungsinstitut für Tiergesundheit, Greifswald-Insel Riems Mentor: Prof. Dr. Martin Beer Gedruckt mit Genehmigung der Tierärztlichen Fakultät der Ludwig-Maximilians-Universität München Dekan: Univ.-Prof. Dr. Reinhard K. Straubinger, Ph.D. Berichterstatter: Univ.-Prof. Dr. Gerd Sutter Korreferent: Priv.-Doz. Dr. Kristina Schauer Tag der Promotion: 25. Juli 2020 Die vorliegende Arbeit wurde gemäß § 6 Abs. 2 der Promotionsordnung für die Tierärztliche Fakultät der Ludwig-Maximilians-Universität München in kumulativer Form verfasst. Folgende wissenschaftliche Arbeiten sind in dieser Dissertationsschrift enthalten: Schulze V, Lurz PWW, Ferrari N, Romeo C, Steele MA, Marino S, Mazzamuto MV, Calvignac-Spencer S, Schlottau K, Beer M, Ulrich RG, Ehlers B „Search for borna-, polyoma-, and herpesviruses in squirrels of the family Sciuridae”, erschienen in Virology Journal 2020, online verfügbar unter doi: 10.1186/s12985-020-01310-4. Schulze V*, Große R*, Fürstenau J, Forth LF, Ebinger A, Richter MT, Tappe D, Mertsch T, Klose K, Schlottau K, Hoffmann B, Höper D, Mundhenk L, Ulrich RG, Beer M, Müller KE, Rubbenstroth D „Borna disease outbreak with high mortality in an alpaca herd in a previously unreported endemic area”, erschienen in Transboundary and Emerging Diseases 2020, online verfügbar unter doi: 10.1111/tbed.13556. Weitere Arbeiten, die nicht in der Dissertationsschrift enthalten sind: Rasche A, Lehmann F, König A, Goldmann N, Corman VM, Moreira-Soto A, Geipel A, van Riel D, Vakulenko YA, Sander AL, Niekamp H, Kepper, R, Schlegel M, Akoua- Koffi C, Souza BFCD, Sahr F, Olayemi A, Schulze V, Petraityte-Burneikiene R, Kazaks A, Lowjaga KAAT, Geyer J, Kuiken T, Drosten C, Lukashev AN, Fichet- Calvet E, Ulrich RG, Glebe D, Drexler JF "Highly diversified shrew hepatitis B viruses corroborate ancient origins and divergent infection patterns of mammalian hepadnaviruses“, erschienen in Proceedings of the National Academy of Sciences of the United States of America 2019, online verfügbar unter doi: 10.1073/pnas.1908072116. Contents 1 Introduction ........................................................................................................ 1 2 Literature review ................................................................................................ 5 2.1. Rodents and other small mammals and their role as reservoirs .................... 7 2.2. Current knowledge on the virus diversity in rodents and other small mammals ............................................................................................................... 10 2.3. Workflows for the identification and genetic characterization of viruses ...... 10 2.3.1. Initiation................................................................................................. 10 2.3.2. General workflows ................................................................................ 11 2.3.3. Sampling and sample preparation ........................................................ 13 2.3.4. Nucleic acid extraction .......................................................................... 13 2.3.5. Molecular methods for initial detection of viruses .................................. 14 2.3.6. Determination of a complete viral genome ............................................ 14 2.4. Orthobornaviruses and their reservoirs ....................................................... 15 2.5. (Non-zoonotic) polyoma- and herpesviruses ............................................... 20 2.5.1. Polyomaviruses ..................................................................................... 20 2.5.2. Herpesviruses ....................................................................................... 22 2.6. Virus-host evolution ..................................................................................... 25 3 Study objectives............................................................................................... 27 3.1. Searching for squirrels as reservoir of the VSBV-1 and for novel polyoma- and herpesviruses in squirrels ............................................................................... 29 3.2. Characterization of the interactions between reservoir host and (accidental) dead-end hosts during an exemplary BoDV-1 outbreak ........................................ 29 4 Results .............................................................................................................. 31 4.1. Publication 1: Search for borna-, polyoma-, and herpesviruses in squirrels of the family Sciuridae ............................................................................................... 35 4.2. Publication 2: Borna disease outbreak with high mortality in an alpaca herd in a previously unreported endemic area in Germany ............................................... 59 5 Discussion ........................................................................................................ 77 5.1. Squirrels as hosts of the Mammalian orthobornavirus 2 .............................. 79 5.2. Novel polyomaviruses in squirrels ............................................................... 80 5.3. Novel herpesviruses in squirrels .................................................................. 83 5.4. Co-infections in squirrels ............................................................................. 84 5.5. The reservoir of BoDV-1 .............................................................................. 85 6 Summary ........................................................................................................... 87 7 Zusammenfassung .......................................................................................... 91 8 References ........................................................................................................ 95 9 Supplement .................................................................................................... 109 9.1. Table S1: Overview about recently discovered viruses associated with rodents and shrews. ............................................................................................ 111 9.2. List of abbreviations ................................................................................... 135 9.3. List of figures ............................................................................................. 139 9.4. List of tables .............................................................................................. 139 10 Acknowledgement ......................................................................................... 141 1 Introduction Chapter 1: Introduction 1 2 1 Introduction 1 Introduction Rodentia is the most numerous and most diversified order of mammals, representing about 43 % of the total number of mammalian species. They are distributed almost worldwide and inhabit a broad range of habitats including forest, desert, agricultural land, and urbanized regions (Wilson, Lacher Jr, and Mittermeier 2016). The order Eulipotyphla, includes more than 400 species, comprising hedgehogs and gymnures (family Erinaceidae), solenodons (family Solenodontidae), the desmans, moles, and shrew-like moles (family Talpidae) and true shrews (family Soricidae), of which the most feed almost exclusively on insects. Equally to rodents they are globally distributed and inhabit all continents, except Antarctica (Wilson and Mittermeier 2018). Due to their close proximity to humans, rodents and insectivores, i.e. shrews, often function as reservoir hosts of numerous zoonotic viruses. They serve as a connection between humans, domestic animals, wildlife and e.g. arthropod vectors (Meerburg, Singleton, and Kijlstra 2009). They can spread viruses either between the respective reservoir hosts or to accidental dead-end hosts. Various molecular methods and workflows have been developed for the identification of novel viruses or virus variants, directly without prior agent cultivation or after virus isolation. The choice of the optimal method depends on the aim of the study, the agents to be detected and their genome organization. Common methods are conventional polymerase chain reactions (PCRs) in different formats (e.g. generic or nested format), quantitative reverse transcription polymerase chain reaction (RT- qPCR) and High-Throughput sequencing (HTS), which can be applied separately or in combination, e.g. in a sophisticated workflow. Even if the implementation of new technologies, like HTS and optimized workflows in combination with classical PCR methods resulted in numerous discoveries of novel viruses in the recent past (Supplement, Table S1), still only a small portion of the whole number of different viruses (so-called ´virome´) in rodents is known (Drewes et al. 2017; Wu et al. 2018). In congruence to this, knowledge about pathogens in squirrels and shrews is also scarce. Therefore, the studies described in this thesis present the characterization of reservoir hosts, exemplary in squirrels and shrews. In addition, results from selected approaches for the
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