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Symbiosis of Parasites in the Blood, Gut and Skin of Cameroonian Bos Taurus and Bos Indicus Cattle

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Symbiosis of Parasites in the Blood, Gut and Skin of Cameroonian Bos Taurus and Bos Indicus Cattle Symbiosis of parasites in the blood, gut and skin of Cameroonian Bos taurus and Bos indicus cattle Dissertation der Mathematisch-Naturwissenschaftlichen Fakultät der Eberhard Karls Universität Tübingen zur Erlangung des Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) vorgelegt von Archile Eric Paguem II aus Ngaoundere, Kamerun Tübingen 2019 i Gedruckt mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät der Eberhard Karls Universität Tübingen. Tag der mündlichen Qualifikation: 05.03.2020. Dekan: Prof. Dr. Wolfgang Rosenstiel 1. Berichterstatter: PD. Dr. Alfons Renz 2. Berichterstatter: Prof. Dr. Oliver Betz i Table of contents Acknowledgements......................................................................................................ii Abbreviations..............................................................................................................iv Summary………………................................................................................................v Zusammenfassung…………….……...........................................................................vii List of publications…………….…….............................................................................ix Author contributions..…………………………………………….………….………..….....x 1- General Introduction……………………………………….…...…….........….1 1.1. Multi-parasites infections……………….…………….….…………...………1 1.1.1 Trypanosoma diversity, potential hosts and life cycles..………..………...2 1.1.2 Onchocera co-infecting cattle…………………………………..…….....…...4 1.1.3 Gastrointestinal helminths and protozoans co-infecting cattle……….…..6 1.2. Factors facilitating multi-parasitism……………..…………….……….…...8 1.2.1 Seasonality and the climatic conditions………….………..………..…….....8 1.2.2 The spatial and temporal distribution………………………..…..……...........9 1.2.3 Host susceptibility………………….………………………….………………..9 1.3. Symbiosis and multi-parasites interactions………………….………..…11 1.3.1 Competition for space and resources…………………….…..……….…..11 1.3.2 Host immunomodulation…………………………………………………….12 1.4. Consequence of multi-parasitism …………………….….…….…….........13 2- Objectives and expected output……….…………….…….………….....14 3- Materials and Methods………………………………..……..……………….16 3.1. Study areas…………………..………..….……….…………….…………….16 3.2. Animal selections…………….………...….………………….…………......17 3.3. Field work and sampling procedure…………….…………...…………….17 3.4. DNA extraction from buffy coat………………..…………………..………22 3.5. Molecular identification of trypanosomes ………………………………23 3.6. Molecular identification of tick-borne bacteria and piroplasmids……23 3.7. Phylogenetic analysis………………………………………………………..23 3.8. Statistical analysis…………………………………………..……………….24 3.9. Whole genome sequencing of taurine and Zebu cattle ….…………….24 3.10. Bovine genotyping ……………………………………………….......……...25 i 4- Results and discussion……………………….………………………….…26 4.1. Component community of blood parasites of naturally infected cattle …………………………………………………………………………………...26 4.1.1. Susceptibility and diversity of trypanosomes……………………………26 4.1.2. Susceptibility and diversity of tick-borne bacteria and piroplasmids…..31 4.1.3. Blood-dwelling filarial parasites (Setaria)………....…………….……..…34 4.2. Component community of gut helminths..…………………………….…35 4.2.1. Susceptibility and diversity of gastro-intestinal helminths infection…...35 4.2.2. Molecular diversity of major Trichostrongylids……………….................39 4.2.3. Diversity of rumen flukes………………..…………………………...……..41 4.3. Component community of skin dwelling Onchocerca microfilariae ……………………………………………………...……………………………45 4.4. Co-infections of helminths, Eimeria oocyst and Trypanosomes.…....49 4.5. Parasite-parasite associations…………………..…………………………51 4.6. Host genetic factors of susceptibility and resistance to multi- parasitism…………….…………………………………………………….….53 4.7.1. Genetic diversity landscape of different cattle breeds using WGS…..…53 4.7.2. Genetic diversity of BoLA (MHC) of different cattle breeds…….……......57 4.7.3. Genetic diversity of BoLA DRB3 (MHC) of different cattle breeds……...61 5- General discussion……………………………..….………..………………..65 5.1. Diversity of parasites infecting cattle……….…………..………………..65 5.2. Co-infections and parasite-parasite associations..…………….……..66 5.3. Facilitating and limiting factors of multi-parasitism………………..…67 5.4. The concept of host territorial defense by parasites…………………..67 5.5. Practical implications………………………….…………………………...68 6- Conclusion……………………………….……………………………...…........69 7- References………………………………….……………………….…...……....70 8- Appendix…………………………….…….……….………..…….……..……....87 ii Acknowledgements First and foremost, I would like to express my sincere gratitude to my supervisors, PD. Dr. Alfons Renz and Prof. Dr. Mbunkah Daniel Achukwi for offering me the opportunity to work on this interesting topic independently with the freedom of pursuing my own research interests. I also wish to thank them for their continuous support, precious advice and constructive criticism throughout this thesis. I am very thankful to Prof. Oliver Betz who kindly accepted to co-supervise my thesis and to Prof. Katharina Förster who provided laboratory facilities in Tübingen. I would like to express my gratitude to PD. Dr. Adrian Streit at Max Planck Institute, Tübingen and Dr. Stefan Czemmel and Dr. Praveen Baskaran from quantitative Biology Center (QBiC) for their wonderful support during my projects. I express my sincere thanks to Prof. Soege Kelm for the warm welcome in his laboratory at Bremen and to his research group members: Dr. Ngomtcho Claudine, Judith Weber, Ibrahim Mahmat and Petra Berger. A big thanks to Prof. Dieudonne Ndjonka from the University of Ngaoundere for his support, suggestions and encouragements and Mme Monika Meinert form Oliver Betz group for Scanning Electron microscopy examination of stomach flukes samples. I greatly acknowledge the support of Dr. Albert Eisenbarth throughout the studies. I would like to thanks all the cattle owners and herdsmen who granted us access to their cattle and participated in the fieldwork survey. To the chief of the IRAD Wakwa center (Dr. Oumarou Palou MADI) and the veterinarians DVM Dr. Kingsley Manchang, Prof. Dr. Mamoudou Abdoulmoumini with whom I collaborated in the fieldwork. I want to thanks my classmate and colleagues Abanda Babette, Nancy Ngwasiri, Daniela Renz and the team of Programme Onchocercoses station in Ngaoundéré with whom I collaborated during the DFG-cobe and QTLs projects. Big thanks go to my funding agencies Deutsche Forschungs Gemeinschaft (DFG-COBE project Re 1536/2-1), Otto-Bayer(F-2013BS522), International Foundation for Sciences (IFS, B/5864-1), the Baden Württemberg Stiftung (BWS- RIK and BWS-plus) and the joint RiSC program of the State Ministry of Science, Research and Arts Baden Württemberg and the University of Tübingen (Eisenbarth, PSP-no. 4041002616) and the DAAD. ii Finally, I want to thank my parents, siblings for their encouragement and support throughout the whole process of my thesis and my friend Isabelle Richard Voniarisoa for putting up with my bad moods and stress. iii Abbreviations AEZ Agro ecological zone BCS Body condition score BoLA Bovine Leucocyte Antigens (equivalent to MHC) Bs-SNPs Breeds-specific Single Nucleotide Polymorphism gGAPDH glycosomal Glyceraldehyde 3-Phosphate Dehydrogenase Genes GWAS Genome Wide Association study HSP70 Heat Shock Protein 70 Indels an Insertions and deletions of bases in the genome of an organism ITS1 Internal Transcript Spacer 1 ITS2 Internal Transcript Spacer 2 PCR Polymerase Chain Reaction PCV Packed Cell Volume QTLS Quantitative Trait Loci rRNA ribosomal RNA S. Setaria s.I. Sensu lato SNP Single Nucleotide Polymorphism spp. Species SSU Small Subunit T. Trypanosoma TBDs Tick-borne diseases TNF Tumour Necrosis Factor WGS Whole genome sequencing iv Summary in English Parasitism is a wide-spread lifestyle adopted by more than 50 % of living organisms on Earth. Under natural conditions, almost every host species is simultaneously infected with multiple parasite species (viruses, bacteria, protozoan, fungi and helminths) over the course of their lifetime. However, our knowledge on interspecific interactions of all the different parasites species that live together have been poorly understood. This symbiotic associations can be either synergistically with mutualistic benefit from parasites and host or antagonistically with elimination of one parasite species or harm to the host. In this thesis, I investigated factors that structure parasite communities with emphasis on symbiosis of parasites in a free ranging population of African indigenous cattle breeds (ca. 1300 animals). The Sudan Savannah and the Sahel habitats of Cameroon are endemic for trypanosomes, tick and tick-borne pathogens, gastro-intestinal helminths and filarial nematodes. In order to get a better understanding of the whole parasite communities, blood, skin and faecal samples of Zebu and taurine cattle were examined using microscopy, PCR and Sanger sequencing. The cattle body condition, live-weight and the haematocrit was measured. As expected, almost all animals were infected with at least one parasite. Using molecular tools, I found seven species of trypanosomes and fifteen tick-borne pathogens (TBD) were found in the blood, co-occurring with the microfilariae of Setaria labiatopapillosa. I found an antagonistic polarizing effect with view to the presence of either pathogenic or non-pathogenic trypanosomes, while mutualistic associations with TBPs lead to protection of cattle against pathogenic TBD and exotic breeds
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