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The Diversity of Coronaviruses in Southern African Bat Populations

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The Diversity of Coronaviruses in Southern African Bat Populations THE DIVERSITY OF CORONAVIRUSES IN SOUTHERN AFRICAN BAT POPULATIONS by Nadine Cronjé Dissertation presented for the degree of Doctor of Philosophy (Medical Virology) in the Faculty of Medicine and Health Sciences at Stellenbosch University Supervisor: Prof. Wolfgang Preiser Co-supervisors: Prof. Corrie Schoeman and Dr Ndapewa Ithete December 2017 Stellenbosch University https://scholar.sun.ac.za The financial assistance of the National Research Foundation (NRF) towards this research is hereby acknowledged. Opinions expressed and conclusions arrived at, are those of the author and are not necessarily to be attributed to the NRF. i Stellenbosch University https://scholar.sun.ac.za Declaration By submitting this dissertation electronically, I declare that the entirety of the work contained therein is my own, original work, that I am the sole author thereof (save to the extent explicitly otherwise stated), that reproduction and publication thereof by Stellenbosch University will not infringe any third party rights and that I have not previously in its entirety or in part submitted it for obtaining any qualification. December 2017 Copyright © 2017 Stellenbosch University All rights reserved ii Stellenbosch University https://scholar.sun.ac.za Summary Coronaviruses are RNA viruses encompassing four genera. The alpha- and betacoronaviruses have commonly been associated with mild disease in humans. However, outbreaks of severe respiratory disease in 2002 and 2012 led to the identification of novel highly pathogenic human coronaviruses, SARS- and MERS-CoV, respectively. Bats, order Chiroptera, are believed to be the reservoir host from which all mammalian coronaviruses have emerged. To date, few studies have been published on coronaviruses in South African bats. With little known about the diversity and prevalence of bat coronaviruses in this region; this study aimed to describe the existing coronavirus diversity within South African bat populations as well as factors that might influence bat-coronavirus ecology. It detected nine different coronavirus species, eight alphacoronaviruses and one betacoronavirus, from ten different bat species. The study not only demonstrated that diverse coronaviruses can be found in different bat species of Southern Africa but lends additional support to an ongoing circulation of MERS-related betacoronaviruses in South African bats, with divergent variants detected in two different vespertilionid bat species. A species-specific surveillance of Neoromicia capensis (Cape serotine) bats detected three different bat coronavirus species and revealed genetic diversity across different geographic regions. Several instances of coinfection with two different coronaviruses were detected, demonstrating the potential for recombination that could lead to the emergence of a new coronavirus that might have zoonotic potential. This study demonstrated that both host and environmental factors may influence CoV ecology. Female Neoromicia capensis bats trapped at low altitude sites within the Forest biome had the highest likelihood of being coronavirus positive. Discrepancies between detection rates obtained with different screening assays led to the adoption of an improved approach and recommendations for future bat coronavirus surveillance studies were made. iii Stellenbosch University https://scholar.sun.ac.za Opsomming Koronavirusse is RNA virusse wat vier genera insluit. Die alfa- en betakoronavirusse word algemeen geassosieer met minder ernstige siektes by mense. Uitbrakings van ernstige respiratoriese siektes in 2002 en 2012 het egter gelei tot die identifisering van nuwe hoogs patogeniese menslike koronavirusse, SARS- en MERS-koronavirus, onderskeidelik. Vlêrmuise, orde Chiroptera, word beskou as die reservoir gasheer, wat tot die oorsprong van alle soogdierkoronavirusse gelei het. Tot dusver is min studies oor koronavirusse in Suid-Afrikaanse vlêrmuise gepubliseer. Met min kennis van die diversiteit en voorkoms van vlêrmuiskoronavirusse in hierdie streek; het hierdie studie ten doel om die bestaande koronavirusdiversiteit binne Suid-Afrikaanse vlêrmuispopulasies asook faktore wat vlêrmuis-koronavirus-ekologie kan beïnvloed, te ondersoek en beskryf. Nege verskillende koronavirus spesies, agt alfakoronavirusse en een betacoronavirus, is in tien verskillende vlêrmuis spesies geïdentifiseer. Die studie het nie net gedemonstreer dat diverse koronavirusse in verskillende vlêrmuise van Suider-Afrika voorkom nie, maar ook addisionele ondersteuning aan 'n deurlopende verspreiding van MERS-verwante betakoronavirusse in Suid- Afrikaanse vlêrmuise verleen, met uiteenlopende variante wat in twee verskillende vespertilioniedvlêrmuise aangetref word. 'n Spesiespesifieke waarneming van Neoromicia capensis (Kaapse serotien) vlêrmuise het drie verskillende koronavirus spesies opgespoor en genetiese diversiteit in verskillende geografiese streke opgemerk.Verskeie gevalle van meervoudige infeksies met twee verskillende koronavirusse is opgemerk, wat die potensiaal vir rekombinasie aantoon, wat kan lei tot „n nuwe koronavirus wat soönotiese potensiaal kan hê. Hierdie studie het getoon dat beide gasheer- en omgewingsfaktore koronavirus ekologie kan beïnvloed. Vroulike Neoromicia capensis vlêrmuise wat voorkom in laagliggende areas in die Woud bioom het die hoogste waarskynlikheid om koronavirus positief te wees. Afwykings tussen opsporingsyfers wat met verskillende siftingsmetodes verkry is, het gelei tot die aanvaarding van 'n verbeterde benadering en aanbevelings vir toekomstige vlêrmuis- koronavirus toesigstudies is gemaak. iv Stellenbosch University https://scholar.sun.ac.za Personal Acknowledgements I have had the privilege of spending the last few years completing my PhD within the Division of Medical Virology. During this time I have gained invaluable research skills and experience. I have learned how to work independently and how to be adaptable in the face of change as is inevitably to be expected when conducting research. For this I am most grateful. Thank you to the staff and students in the Division of Medical Virology for every friendly smile, chit- chat, and cup of tea shared. Your support and encouragement is appreciated. Thank you to our collaborators, Prof. Corrie Schoeman (University of KwaZulu-Natal) and Dr Leigh Richards (Durban Natural History Museum), and their respective field teams, for collecting study samples and for accommodating my many requests. A special thank you must go to Karmistha Poovan for her friendship and constant support. Thank you for putting up with my endless questions, moments of crises, and requests to “quickly run something by you”, you are the epitome of a true friend! To Dr Ndapewa Ithete, thank you for your willingness to serve as a co-supervisor on this study. I have not only learned a great deal of practical knowledge from you but also how to teach and guide others with patience and kindness. A huge thank you must go to Prof. Corrie Schoeman for your co-supervision. Thank you for exposing me to the world of bats and ecology and for broadening my understanding of the wider subject within which my study falls. Your expertise has been invaluable and I am grateful for all that I have learned from you. Thank you for convincing me to get out into the field - the fieldwork expeditions certainly created some of my most memorable memories! An enormous thank you must go to Prof. Wolfgang Preiser for supervising me. Your guidance, encouragement, input, and support have been invaluable to the success of this study. Thank you for sharing your wealth of knowledge and expertise with me – I have never not left having learned something new after chatting to you. You have greatly facilitated my growth as a scientific researcher during this journey and for that I am most grateful. To my dear parents, Wayne and Erica, thank you for your unending love and support, and for always believing in me. You have continuously inspired and motivated me to follow my dreams - I could not have asked for better parents, thank you. Friends and family, near and afar, your support during this journey is greatly appreciated – I could not have done this without all the encouragement along the way. Lastly, thanks must go to my loving husband, Ludi, for your unwavering love, support and motivation – you continue to be my number one fan! Thank you for all the encouragement and patience throughout the madness of it all. Thank you for keeping me well-fed and happy – your uncanny ability to make me laugh each day has certainly made the challenging days more bearable. The journey has been a long one but so much more enjoyable with you by my side. v Stellenbosch University https://scholar.sun.ac.za Formal Acknowledgements Individual Institute Contribution Dr Leigh Richards Durban Natural History collection and provision of loaned sample Museum material Dr Ndapewa Ithete Division of Medical Virology, provision of RGU_2c primers Stellenbosch University Dr Tasnim Suliman Division of Medical Virology, provision of primers for extended Stellenbosch University amplification of lineage C betacoronaviruses Mr Quartus Laubscher Private monthly collection of samples from a bat colony on his property Prof. Corrie Schoeman School of Life Sciences, collection and provision of study samples; University of KwaZulu-Natal provision of R code for biogeographic analyses Central Analytical Facility: sequencing electrophoresis DNA Sequence Unit, Stellenbosch University South African Weather provision of requested weather data. Service German Research
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