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High-Throughput Sequencing As a Tool for Studying Strongylid Nematode Communities in Primates

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High-Throughput Sequencing As a Tool for Studying Strongylid Nematode Communities in Primates Faculty of Science High-throughput sequencing as a tool for studying strongylid nematode communities in primates Diploma thesis Bc. Vladislav Ilík Supervisor: Mgr. Barbora Pafčo, Ph.D. Department of botany and zoology Field of study: Zoology Brno 2020 1 Přírodovědecká Fakulta Velkokapacitní sekvenování jako nástroj studia strongylidních hlístic u primátů Diplomová práce Bc. Vladislav Ilík Vedoucí práce: Mgr. Barbora Pafčo, Ph.D. Ústav botaniky a zoologie obor Zoologie Brno 2020 2 3 Bibliografický záznam Autor: Bc. Vladislav Ilík Přírodovědecká fakulta Masarykova univerzita Ústav botaniky a zoologie Název práce: Velkokapacitní sekvenování jako nástroj studia strongylidních hlístic u primátů Studijní program: Zoologie Studijní obor: Zoologie Vedoucí práce: Mgr. Barbora Pafčo, Ph.D. Rok: 2020 Počet stran: 101 Klíčová slova: Nematoda; Strongylida; Společenstvo; Člověk; Gorila; Šimpanz; Přenos; Zoonóza; Velkokapacitní sekvenování; ITS-2 4 Bibliographic entry Author: Bc. Vladislav Ilík Faculty of Science Masaryk University Department of Botany and Zoology Title of Thesis: High-throughput sequencing as a tool for studying strongylid nematode communities in primates Degree Programme: Zoology Field of Study: Zoology Supervisor: Mgr. Barbora Pafčo, Ph.D. Year: 2020 Number of pages: 101 Keywords: Nematoda; Strongylida; Community; Human; Gorilla; Chimpanzee; Transmission; Zoonosis; High-throughput sequencing; ITS-2 5 Abstrakt Úvod Strongylidní hlístice patří k nejdůležitějším patogenům suchozemských obratlovců, včetně lidí a primátů. Více než 400 milionů lidí celosvětově je nakaženo měchovci, kteří mají významné ekonomické a zdravotní dopady, zejména v rozvojových zemích. V posledních desetiletích zaznamenává lidská populace nebývale vysoký nárůst a rozšíření lidských sídel. Naopak, u volně žijících divokých zvířat dochází spíše k populačním poklesům a vykořisťování z jejich původně přirozeného prostředí. Těžba dřeva, lov a zemědělství jsou dnes hlavními příčinami poklesu biodiverzity. Vzrůstající lidský kontakt s divokými zvířaty však s sebou přináší riziko vzájemné výměny a sdílení některých patogenů. V Africe lidé často žijí v malých, místních komunitách a v úzkém soužití s divokými zvířaty. Jejich životní styl stále zůstává pre-industriální a zaměřený spíše na tradiční způsoby obživy, jako je lov, sběr či jednoduché zemědělství. Jelikož jsou primáti úzce fylogeneticky příbuzní lidem, předpokládá se, že mezi nimi bude docházet k vzájemné výměně patogenů. Obzvláště, když strongylidní hlístice představují tvoří dominantní složku jejich parazitofauny. Metodika a výsledky V této studii jsem využil jsem velkokapacitní sekvenování (HTS) jako nástroj ke studiu a popisu společenstev strongylidních hlístic u lidí a primátů, společně obývajících severní okraj přírodní rezervace DJA v Kamerunu. Výsledky přibližně odpovídají výsledkům předchozích studií, jelikož u rodů Oesophagostomum a Necator byly zaznamenány nejvyšší prevalence a primáti vykazovali větší diverzitu parazitofauny než lidé. Velkokapacitní sekvenování také zachytilo přítomnost vzácných, jinak opomíjených taxonů jako Ancylostoma, Ternidens a Trichostrongylus. Navíc odhalilo přítomnost několika zoonotických haplotypů, sdílených mezi lidmi a primáty. U primátů běžně přítomné O. stephanostomum bylo zaznamenáno i u lidí. Zároveň jsem odhalil jeden přítomnost rodu Trichostrongylus u všech studovaných druhů, avšak u lidí byl zaznamenán pouze v jednom případě. Necator americanus, původně označován jako lidský parazit, byl nalezen u lidí i u goril. Na druhou stranu, N. gorillae, původně popsán u goril nížinných, byl nalezen u všech hostitelských druhů. 6 Závěr Výsledky této studie rozšiřují aktuální znalosti o komplexních společenstvech strongylidních hlístic. Také podtrhují stále rostoucí trend, kdy dochází k nárůstu lidského kontaktu s divokými zvířaty a vzájemnému přenosu patogenů. Kvůli nepopiratelnému významu některých popsaných parazitů by mělo být v budoucnu vloženo úsilí do minimalizování kontaktu a přenosů, jelikož důsledky mohou být vážné na obou stranách. I když jsou paraziti primátů často ve vědeckém “hledáčku”, pouze málo je známo o komplexních společenstvech které tvoří, a proto mohou představovat vhodné organismy pro budoucí výzkum. Závěrem, velkokapacitní sekvenování (HTS), aplikované na směsné vzorky ze stolice představuje levný a rychlý způsob k nahlédnutí nejen do diverzity strongylidních hlístic. Navíc s vyšší rozlišovací schopností než za použití tradičních postupů. Aplikace této metody boří hranice klasického Sangerova sekvenování a umožňuje analýzu hostitelské specifity strongylidních hlístic ve složitých parazito- hostitelských vztazích. 7 Abstract Introduction Strongylid nematodes belong to one of the most important pathogens of terrestrial vertebrates, including humans and non-human primates. Hookworms alone infect over 400 million people wordlwide, bringing significant economic losses and public health concerns, especially in developing countries. In past decades, human population is recording unprecedented rapid growth and expansion of the human settlements. On the contrary, wild, free-living animals are going through the exact opposite trend with generally decreasing populations and forcing out of their (once natural) habitats. Logging, hunting and agriculture are the main driving forces standing behind the global biodiversity decrease. Intensified human contact with wildlife, however, brings along a risk of mutual pathogen exchange and sharing. Great apes are phylogenetically closely related to humans, therefore pathogen exchange is presumed, especially with strongylid nematodes being dominant parasites of both humans and great apes. Methodology and principal findings In this study, I used metabarcoding ITS-2 high-throughput sequencing (HTS) approach as a tool for evaluation of strongylid nematode communitites and the zoonotic potential between humans and great apes cohabiting the northern periphery of the DJA Faunal Reserve in Cameroon. The results were relatively consistent with previously conducted studies, as I found Oesophagostomum and Necator being the most prevalent genera. Moreover, great apes exhibiting greater diversity of parasite fauna than humans. In addition, the HTS approach captured presence of the rare, often neglected taxa, such as Ancylostoma, Ternidens and Trichostrongylus as well as closely unidentified strongylid nematodes. HTS revealed several zoonotic haplotypes being shared between humans and great apes. There was evidence of O. stephanostomum (commonly found in great apes) in humans. Necator americanus, formerly believed to be a human-specific parasite, was found in humans and gorillas. On the contrary, N. gorillae, originally described in western lowland gorilla was found to be widespread across all host species. Last, a single haplotype of closely unidentified Trichostrongylus was also found to be shared across all studied hosts, however, only one human was infected. 8 Conclusion The results of this study brought additional knowledge to the understanding of complex strongylid nematode communities. They also underline the growing trend of intensified human contact and mutual pathogen exchange. Due to the indisputable importance of some described parasites, there should be put some efforts to minimise the contact and transmission events as it can have consequences on both sides. Even though primate parasites are often under scientific “finderscope”, little is known about their parasite communitites and therefore they may represent suitable organisms for future scientific studies and focus. In conclusion, high-throughput sequencing of strongylid nematodes from fecal samples represent a time- and cost-efficient way of studying helminth communitites and provides a resolution superior to traditional approaches. Its application overcomes the limitations of classical Sanger sequencing and allows for analyses of strongylid nematode host-specifity in complex parasite-host systems. 9 10 11 Čestné prohlášení Prohlašuji, že jsem svoji diplomovou práci vypracoval samostatně pod vedením vedoucího práce s využitím informačních zdrojů, které jsou v práci citovány. V Brně 19. května 2020 ....................................... Bc. Vladislav Ilík 12 Acknowledgements Hereby, I would like to thank primarily my dearest supervisor Dr. Barbora Pafčo, especially for her constant “24/7” support and warm, human-kind attitude. She introduced me the mysteries of the “scientific world”, helped with the laboratory work and gave me valuable contacts. Finally, she helped me propose the life-changing opportunity to spend a whole year in the USA as I am a successful Fulbright scholar. Although I was pretty sceptical about possible success in the beginning. I am fully aware of the amount of the time and effort she put into me and I strongly hope that my following work (and the work during the time of our collaboration) will bring a dignifying result. I would like to also thank my co-supervisor Dr. Martin Kašný, who introduced me to the HPI-Lab team and helped me with finalising this thesis. The last person who contributed significantly to my work is Dr. Jakub Kreisinger, who prepared the basic dataset and helped me a lot with bioinformatic processing of the data. Therefore, I would like to express my gratitude to him. I also express my gratitude to all members of the HPI-Lab Team, who accepted me into the collective, and for me, it was a pleasure to work with them (I hope for them as well). Namely: the “chieftain” of our team, prof. David Modrý, the main coordinator
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