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New Molecular High Throughput Methods for Ehrlichia Ruminantium Tick Screening and Characterization of Strain Genetic Structure in Mozambique and at Worldwide Scale

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New Molecular High Throughput Methods for Ehrlichia Ruminantium Tick Screening and Characterization of Strain Genetic Structure in Mozambique and at Worldwide Scale New molecular high throughput methods for Ehrlichia ruminantium tick screening and characterization of strain genetic structure in Mozambique and at worldwide scale Nídia Cangi Thesis presented on the 30th of January 2017 to obtain the grade of Doctor of Philosophy in Life Science, speciality in Molecular biology and Genetics, from the Université des Antilles Jury members: Reviewer: Prof. Christine MARITZ-OLIVIER Reviewer: Dr Eric DUCHAUD Examiner: Dr Nicola COLLINS Examiner: Prof. Jérôme GUERLOTTE Guest members: Thesis director: Prof. Olivier GROS Thesis co-director: Prof. Luís NEVES Thesis co-director: Dr Nathalie VACHIÉRY Acknowledgments I would like to express my gratitude to several people and institutions that contributed directly and indirectly to complete this thesis. I would like to thank sincerely my supervisors Dr Nathalie Vachiéry and Prof. Luís Neves for all their support and guidance, teaching, kindness and especially patience throughout the project. I would not be able to cross the many barriers on my way without their helping hands. I also would like to thank all members of CIRAD-Guadeloupe for receiving me, for their friendship, ideas and help in times of need, especially to Laure Bournez, Soledad Castano, Valerie Pinarello, Rosalie Aprelon, Christian Sheikboudou, Isabel Marcelino, Emmanuel Albina, as well as Adela Chavez, Jonathan Gordon and Mathilde Gondard. To CB-UEM for contributing to my academic development and to my supportive and friendly colleagues. To Prof. Olivier Gros and the University of Antilles for all the administrative support. To all my family and friends, especially my mother Balbina Müller and my husband Nilton Vaz that even without understanding the science behind my work always encouraged and loved me. I am grateful to Hermógenes Mucache, Laure Bournez and Prof. Luís Neves for all the great field trips in our beautiful Mozambique, friendship and support. As well as the Veterinary Services of Mozambique, Coutada de caça 11 and 12 in Sofala and the Veterinary staff of the KNP and SAN Parks (South Africa) for logistic support during sampling. To God and the Universe for protecting and illuminating my way. To me, for all my patience, persistence, sacrifice, for all the personal growth, strength to not give up and to recover from mental fatigue and tendinitis. I succeed! Last, I would like to thank IRD-Doctorants du Sud (Institut de recherche pour le développement), Ministry of Science and Technology in Mozambique, French Embassy in Mozambique, CIRAD and CB-UEM for providing funds, without which this study would not have been possible. i Summary Ehrlichia ruminantium is the causal agent of heartwater, a ruminant tropical fatal disease transmitted by Amblyomma ticks. Up to now, no effective vaccine is available due to a limited cross protection of vaccinal strains on field isolates mainly associated to a high genetic diversity of E. ruminantium within geographical locations. Thus, both characterization of E. ruminantium genetic population structure at worldwide and regional scale and estimation of E. ruminantium tick prevalence are important to delimitate better control strategies and improve heartwater monitoring strategies. In Section I, we developed two new qPCRs, pCS20 Sol1TM and Sol1SG, to screen E. ruminantium in Amblyomma ticks, which are powerful tools for: 1) heartwater epidemiological studies, 2) diagnosis in the context of heartwater clinical cases and 3) follow-up of experimental infections, both in ticks and hosts. The pCS20 Sol1TM qPCR was found as sensitive (up to 30 copies/sample) and specific as the gold standard pCS20 nested PCR but less prone to sample contamination and less time-consuming. The whole method including the automated DNA extraction and pCS20 Sol1TM qPCR demonstrated to be sensitive, specific and reproducible. It displayed the same limit of detection of the manual DNA extraction and pCS20 nested PCR, (60 copies/sample). Moreover, the development of a high-throughput automated DNA/RNA extraction makes the screen of any tick-borne pathogen in several tick species possible. The development of this new method allowed processing of a high number of tick samples collected in Mozambique that were then typed by Multi Locus Sequence Typing (MLST) and included into a worldwide E. ruminantium strain genetic structure study (Section II). Our study reveals the repeated occurrence of recombination between E. ruminantium genotypes and its important role in E. ruminantium genetic diversity and evolution. Despite the unclear phylogeny and phylogeography due to recombination events, E. ruminantium isolates are clustered into two main groups: Group 1 (West Africa) and a Group 2 (worldwide) which is represented by West, East and South Africa, Indian Ocean and Caribbean strains. Common genotypes between West Africa and Caribbean and Southern Africa and Indian Ocean allow to identify two possible ways of E. ruminantium introduction in these regions, associated with cattle movement. ii In Section III, we focused mainly on E. ruminantium tick prevalence and genetic diversity and structure of Mozambican isolates from A. variegatum and A. hebraeum ticks collected in cattle and wildlife. Sampling was performed in 30 localities for Mozambique and in Kruger National Park (KNP, South Africa). E. ruminantium tick prevalence in cattle was between 0% [0-23.2 %] and 26.7% [12-45 %], with no infected ticks in 7 localities. In wildlife, tick prevalence was 8.2 [4-14.6 %] % in the KNP and 6.2% [0.2-30.2 %] in hunting concessions of Sofala province. However, no significant difference in prevalence was found between sampling sites and tick species, as well as no linear correlation between E. ruminantium prevalence and tick abundance was observed. There was a high genetic diversity of E. ruminantium, with 39 different genotypes detected and distribution of identical genotypes in several distant localities. Most genotypes from Mozambique clustered in genetic subgroup G2C (strictly clustering Zimbabwe and Mozambican isolates) and G2E. Interestingly, genotypes from group G1 and G2D associated mainly with West Africa and Caribbean strains were in minority, probably highlighting a recent introduction. iii iv Table of contents I. Introduction……………………………………………………………………………1 1. Heartwater………………………………………………………………………………...2 1.1. Pathogen: Ehrlichia ruminantium……………………………………………………………….2 1.2. Life cycle………………………………………………………………………………………...2 1.3. The disease: Heartwater…………………………………………………………………………3 1.4. Heartwater in Mozambique……………………………………………………………………...4 1.5. Affected animals…………………………………………………………………………………4 1.6. Geographic distribution………………………………………………………………………….6 1.7. Vector species……………………………………………………………………………………7 2. Molecular diagnostic………………………………………………………………............7 2.1. DNA extraction of tick and tissue samples for screening E. ruminantium………………………7 2.2. Heartwater diagnostic and Ehrlichia ruminantium detection methods…………………………..8 3. E. ruminantium genetic characterization…………………………………………………12 3.1. PCR and restriction fragment length polymorphism (RFLP)…………………………………...12 3.2. Multi-locus variable numbers of tandem repeats (MLVA)……………………………………..13 3.3. Multilocus sequence typing (MLST)……………………………………………………………14 3.4. Importance of recombination events…………………………………………………………….15 II. Aims of the study……………………………………………………………………....17 III. Section I………………………………………………………………………………...19 Efficient high throughput molecular method to detect Ehrlichia ruminantium in ticks (Article 1: submitted to Parasites & Vectors) IV. Section II……………………………………………………………………………….63 Recombination is a major driving force of genetic diversity in theAnaplasmataceae Ehrlichia ruminantium (Article 2: published in Frontiers in Cellular and Infection Microbiology) V. Section III……………………………………………………………………………...64 Ehrlichia ruminantium in Mozambique: a study on prevalence in ticks and isolate genetic diversity (Draft in preparation for publication) VI. General discussion…………………………………………………………………….91 VII. Conclusions and perspectives…………………………………………………….......99 VIII. References…………………………………………………………………………….102 IX. Annexe………………………………………………………………………………...117 Parapatric distribution and sexual competition between two tick species, Amblyomma variegatum and A. hebraeum (Acari, Ixodidae), in Mozambique (Published in Parasites & Vectors) v Introduction I. Introduction 1 Introduction 1. Heartwater 1.1. Pathogen: Ehrlichia ruminantium In 1925, Edmund Cowdry named the causal agent of heartwater Rickettsia ruminantium (Cowdry, 1925a, Cowdry, 1925b). Later, based on cytological studies, the microorganism was renamed Cowdria ruminantium by Moshkovski (1947). Further studies on the biology of the bacteria cultured in bovine umbilical endothelial cells showed that they have a life cycle similar to that of chlamydia species (Jongejan et al., 1991b). With the advance of molecular biology, the 16S rDNA gene from C. ruminantium was sequenced and a close phylogenetic relation between the genera Cowdria and Ehrlichia was demonstrated (van Vliet, Jongejan & van der Zeijst, 1992). Later, the taxonomy and classification of the order Rickettsiales was clarified with the development of molecular phylogeny, based on the 16S rRNA gene, groESL gene and surface protein genes (Dumler et al., 2001). Distinctly, the obligatory intracellular bacteria Ehrlichia ruminantium belongs to the class Alphaproteobacteria, order Rickettsiales and family Anaplasmataceae. The genus Ehrlichia from the family Anaplasmataceae includes the Gram- negative E. (previously Cowdria) ruminantium,
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