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Revisiting the Pneumocystis host specificity paradigm and transmission ecology in wild Southeast Asian rodents

Latinne Alice, Chen Hsuan-Wien, Kuo Chi-Chien, Lorica Renee, Singleton Grant, Stuart Alex, Malbas Fedelino F., Demanche Christine, Chabé Magali, Michaux Johan, Morand Serge. 2021. Revisiting the Pneumocystis host specificity paradigm and transmission ecology in wild Southeast Asian rodents. Infection, Genetics and Evolution, 93:104978, 13 p.

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Quartile : Q2, Sujet : INFECTIOUS DISEASES

Liste HCERES des revues (en SHS) : oui

Thème(s) HCERES des revues (en SHS) : Anthropologie-Ethnologie

Résumé : Pneumocystis fungi are opportunistic parasites of mammalian lungs whose evolution, ecology and host specificity in natural host populations remain poorly understood and controversial. Using an extensive collection of 731 lung samples from 27 rodent species sampled in five Southeast Asian countries, and nested PCR amplification of mitochondrial and nuclear genes, we investigated the host specificity and genetic structure of Pneumocystis lineages infecting wild rodents. We also identified the rodent species playing a central role in the transmission of these parasites using network analysis and centrality measurement and we characterized the environmental conditions allowing Pneumocystis infection in Southeast Asia using generalized linear mixed models. Building upon an unprecedented Pneumocystis sampling from numerous rodent species belonging to closely related genera, our findings provide compelling evidence that the host specificity of Pneumocystis lineages infecting rodents is not restricted to a single host species or genus as often presented in the literature but it encompasses much higher taxonomic levels and more distantly related rodent host species. The phylogenetic species status at both mitochondrial and nuclear genetic markers of at least three new Pneumocystis lineages, highly divergent from Pneumocystis species currently described, is also suggested by our data. Our models show that the probability of Pneumocystis infection in rodent hosts is positively correlated to environmental variables reflecting habitat fragmentation and landscape patchiness. Synanthropic and habitat-generalist rodents belonging to the Rattus, Sundamys and Bandicota genera played a role of bridge host species for Pneumocystis spreading in these heterogeneous habitats, where they can reach high population densities. These are critical findings improving our understanding of the ecology of these enigmatic parasites and the role played by cospeciation and host switches in their evolution. Our results also confirmed the role of land-use change and habitat fragmentation in parasite amplification and spillover in rodents.

Mots-clés Agrovoc : rongeur, Bandicota, hôte, évolution, génétique mitochondriale, habitat, écologie, parasite, marqueur génétique, Pneumocystis, transmission des maladies, modélisation environnementale, parasitisme, fragmentation de l'habitat

Mots-clés géographiques Agrovoc : Asie du Sud-Est

Mots-clés libres : Pneumocystis, Rodents, Southeast Asia, Muridae, Host specificity, Habitat fragmentation

Agences de financement hors UE : Agence Nationale de la Recherche

Projets sur financement : (FRA) Ecologie des communautés rongeurs - pathogènes en Asie du Sud-Est : effets des changements de biodiversité et implications pour l'écologie de la santé, (FRA) Impacts et perceptions locales des changements globaux : santé, biodiversité et zoonoses en Asie du Sud-Est, (FRA) Scénarios de la santé en Asie du Sud-Est: changements d'utilisation des terres, changement climatique et maladies infectieuses

Auteurs et affiliations

  • Latinne Alice, Université de Liège (BEL) - auteur correspondant
  • Chen Hsuan-Wien, National Chiayi University (TWN)
  • Kuo Chi-Chien, National Taiwan University (TWN)
  • Lorica Renee, IRRI [International Rice Research Institute] (PHL)
  • Singleton Grant, IRRI [International Rice Research Institute] (PHL)
  • Stuart Alex, IRRI [International Rice Research Institute] (PHL)
  • Malbas Fedelino F., Research Institute for Tropical Medicine (PHL)
  • Demanche Christine, Université de Lille (FRA)
  • Chabé Magali, Université de Lille (FRA)
  • Michaux Johan, CIRAD-BIOS-UMR ASTRE (FRA)
  • Morand Serge, CNRS (THA) ORCID: 0000-0003-3986-7659

Source : Cirad-Agritrop (https://agritrop.cirad.fr/607090/)

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