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Écologie et évolution de coronavirus dans des populations de chauves-souris des îles de l’ouest de l’océan indien

Authors: Joffrin, Léa;

Écologie et évolution de coronavirus dans des populations de chauves-souris des îles de l’ouest de l’océan indien

Abstract

Les zoonoses représentent 60% des maladies infectieuses émergentes, et 70% de ces zoonoses proviennent de la faune sauvage. Les chauves-souris sont les hôtes de nombreux agents infectieux, notamment de virus responsables de zoonoses chez l’Homme comme le virus Ebola, le virus Nipah ou le virus Hendra. Au cours des deux dernières décennies, de nouveaux virus issus des chauves-souris ont émergé dans les populations humaines et animales, avec des conséquences importantes pour la santé publique, vétérinaire, mais également pour l’économie. C’est notamment le cas des coronavirus (CoVs) tels que le syndrome respiratoire aigu sévère (SRAS), le syndrome respiratoire du Moyen-Orient (MERS) et le syndrome de diarrhée aiguë du porc (SADS), responsables de plusieurs milliers de décès humains ainsi que d’une mortalité élevée dans les élevages porcins. Bien que de nombreuses études aient identifié des CoVs de chauves-souris dans le monde, les connaissances actuelles sur la diversité et les risques associés à l'émergence de CoVs dans les écosystèmes insulaires tropicaux restent à évaluer avec précision. L’objectif de cette thèse était d’étudier l’écologie et l’évolution de coronavirus dans des populations de chauves-souris. Dans un premier temps, nous nous sommes intéressés au niveau d’exposition des hôtes aux CoVs, et à l’histoire évolutive de ces virus dans le contexte phylogéographique des îles de l’ouest de l’Océan Indien. Basée sur l’analyse de 1088 échantillons par biologie moléculaire, cette étude a mis en évidence, pour la première fois, la présence de CoV chez des chauves-souris insectivores à Mayotte, au Mozambique, à l’île de La Réunion, et à Madagascar. La prévalence globale de chauves-souris infectées par les CoVs était de 8,0% ± 1,2% avec une variation significative entre l’Afrique continentale et les îles, mais aussi entre familles de chauves-souris. Nous avons identifié une grande diversité génétique de α-CoVs et de β-CoVs, dont certains sont phylogénétiquement proches de CoVs humains (e.g. HCoV-NL63, HCoV-229E, MERS-CoV). Enfin, ces CoVs sont structurés phylogénétiquement par famille de chauves-souris, supportant une longue histoire de coévolution entre chauves-souris et leurs CoVs dans l’Océan Indien occidental. Nous avons dans un second temps réalisé une étude longitudinale sur la dynamique d’infection de CoV dans une colonie de maternité de Petit Molosse (Mormopterus francoismoutoui), espèce endémique de La Réunion. Basé sur la détection du génome viral dans des prélèvements environnementaux (fèces et guano), nous avons exploré l’effet de la structure de la population sur la dynamique d’infection pendant deux années consécutives. Les résultats montrent une variation très marquée des prévalences d’infection chez les chauves-souris au cours de la saison, avec la présence de deux pics d’infection : lors de la colonisation de la grotte de maternité (associé à une augmentation de la densité des hôtes), et environ un mois après le début de la parturition (associé à la perte d’immunité chez les nouveaux-nés). L’ensemble de ces travaux montre que l’évolution des CoVs des chauves-souris de l’ouest de l’Océan Indien est majoritairement due à de la coévolution entre les hôtes et leurs virus, bien que le contexte insulaire puisse également induire de la spéciation intra-île, au sein des familles de chauves-souris. La mise en évidence de facteurs écologiques et biologiques influant sur la dynamique d’infection à l’échelle d’une population souligne que les risques de transmission de CoVs à d’autres hôtes diffèrent en fonction des communautés de chauves-souris présentes sur chaque île, mais aussi de la structure des populations des hôtes et de sa variation temporelle.

Zoonoses account for 60% of emerging infectious diseases, among which 70% originate from wildlife. Bats host many infectious agents, including viruses responsible for zoonoses in humans such as Ebola, Nipah or Hendraus. For the last two decades, new bat viruses have emerged in human and animal populations, causing major threats for public and animal health. Coronaviruses (CoV) such as Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS) and Acute Acute Diarrhea Syndrome (SADS) are responsible for thousands of deaths in humans and pigs. Although many studies have described bat CoVs around the world, current knowledge about the diversity and risks associated with emerging CoVs in island ecosystems remain to be precisely assessed.In this work, we investigated the ecology and evolution of coronaviruses in bats by assessing the level of bat exposure to CoVs, and the evolutionary history in the phylogeographic context of the islands of the Western Indian Ocean. Based on the molecular screening of 1088 samples, we report, for the first time the presence of CoVs in insectivorous bats on Mayotte, on Madagascar, in Mozambique and on Reunion Island. The overall prevalence of bats positive for CoV was 8.0% ± 1.2%, with significant variation between continental Africa and islands, as well as between bat families. We found a large diversity of α-CoVs and β-CoVs, some being genetically related to those detected in human (e.g. HCoV-NL63, HCoV-229E, MERS-CoV). These CoVs were phylogenetically structured by bat family, supporting a long history of co-evolution between bats and their associated CoVs in the region. We then focused on the Reunion free tailed bat (Mormopterus francoismoutoui), an endemic species on this island, and investigated temporal infection dynamics in a maternal colony, during two consecutive years. Results highlighted a major variation in the prevalence of infected bats during the maternity season, with patterns similar for both years and the presence of two peaks of infection. Indeed, one pic occurs during the colonization of the maternity colony (associated to an increase in host density), and another about a month after the beginning of parturition (potentially associated to a loss of maternal antibodies in newborns). This work provides strong support for a long history of coevolution between bats and their CoVs in the Western Indian ocean, although within-island speciation for each bat families also occurs. Ecological and biological factors influencing the infection dynamics highlights a different level of CoV transmission risks to other hosts, including humans, associated to bat communities inhabiting each island, as well as to temporal variations in host population structure.

Country
France
Keywords

Coronavirus, Épidémiologie, [SDV.EE]Life Sciences [q-bio]/Ecology, environment, [SDV.EE] Life Sciences [q-bio]/Ecology, environment, Chauves-Souris, Epidemiology, Bats, Écologie insulaire, [SDV.BBM] Life Sciences [q-bio]/Biochemistry, Molecular Biology, Coévolution, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Island ecology, Coevolution

Rivera, R., Nollens, H. H., Venn-Watson, S., Gulland, F. M. D., & Wellehan, J. F. X. (2010). Seltmann, A., Corman, V., Rasche, A., Drosten, C., Czirjak, G., Bernard, H., … Voigt, C. (2017).

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  • citations
    This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
    0
    popularity
    This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
    Average
    influence
    This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
    Average
    impulse
    This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
    Average
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citations
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
0
Average
Average
Average
Funded by
EC| RUN-EMERGE
Project
RUN-EMERGE
Supporting the research potential on emerging infectious diseases in La Réunion Island, an EU outermost region in the South-Western Indian Ocean
  • Funder: European Commission (EC)
  • Project Code: 263958
  • Funding stream: FP7 | SP4 | REGPOT
Related to Research communities
COVID-19
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