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Highly Rearranged Mitochondrial Genome in Nycteria Parasites (Haemosporidia) from Bats

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Highly Rearranged Mitochondrial Genome in Nycteria Parasites (Haemosporidia) from Bats Highly rearranged mitochondrial genome in Nycteria parasites (Haemosporidia) from bats Gregory Karadjiana,1,2, Alexandre Hassaninb,1, Benjamin Saintpierrec, Guy-Crispin Gembu Tungalunad, Frederic Arieye, Francisco J. Ayalaf,3, Irene Landaua, and Linda Duvala,3 aUnité Molécules de Communication et Adaptation des Microorganismes (UMR 7245), Sorbonne Universités, Muséum National d’Histoire Naturelle, CNRS, CP52, 75005 Paris, France; bInstitut de Systématique, Evolution, Biodiversité (UMR 7205), Sorbonne Universités, Muséum National d’Histoire Naturelle, CNRS, Université Pierre et Marie Curie, CP51, 75005 Paris, France; cUnité de Génétique et Génomique des Insectes Vecteurs (CNRS URA3012), Département de Parasites et Insectes Vecteurs, Institut Pasteur, 75015 Paris, France; dFaculté des Sciences, Université de Kisangani, BP 2012 Kisangani, Democratic Republic of Congo; eLaboratoire de Biologie Cellulaire Comparative des Apicomplexes, Faculté de Médicine, Université Paris Descartes, Inserm U1016, CNRS UMR 8104, Cochin Institute, 75014 Paris, France; and fDepartment of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697 Contributed by Francisco J. Ayala, July 6, 2016 (sent for review March 18, 2016; reviewed by Sargis Aghayan and Georges Snounou) Haemosporidia parasites have mostly and abundantly been de- and this lack of knowledge limits the understanding of the scribed using mitochondrial genes, and in particular cytochrome evolutionary history of Haemosporidia, in particular their b (cytb). Failure to amplify the mitochondrial cytb gene of Nycteria basal diversification. parasites isolated from Nycteridae bats has been recently reported. Nycteria parasites have been primarily described, based on Bats are hosts to a diverse and profuse array of Haemosporidia traditional taxonomy, in African insectivorous bats of two fami- parasites that remain largely unstudied. There is a need to obtain lies, Nycteridae and Rhinolophidae (12). The type species of more molecular data from chiropteran parasites. Such data would the genus Nycteria is Nycteria medusiformis, first described help to better understand the evolutionary history of Haemosporidia, from Kenya by Garnham and Heisch in 1953 (13) from the ’ which notably include the Plasmodium parasites, malaria s agents. Egyptian slit-faced bat (Nycteris thebaica). Later, this species, We use next-generation sequencing to obtain the complete mito- N. medusiformis, was reported in other species of Nycteris, in- chondrial genome of Nycteria parasites from African Nycteris grandis (Nycteridae) and Rhinolophus alcyone (Rhinolophidae) and cluding the large slit-faced bat, Nycteris grandis (14). A total of six Asian Megaderma spasma (Megadermatidae). We report four species have so far been described in the genus Nycteria (14). complete mitochondrial genomes, including two rearranged mito- To contribute to the identification and characterization of chondrial genomes within Haemosporidia. Our results open out- Nycteria parasites in bats and to ascertain the reasons for the looks into potentially undiscovered Haemosporidian diversity. failure of PCR amplification in previous studies, we have used deep next-generation sequencing (NGS) to assemble the com- cytochrome b | evolution | phylogeny | Nycteris plete mitochondrial genome of four different Nycteria species: N. medusiformis and Nycteria sp. (mixed infection) from N. grandis aemosporidia blood parasites (phylum Apicomplexa) are (Nycteridae); Nycteria gabonensis from Rhinolophus alcyone Hvector-borne protozoan parasites that infect multiple ver- (Rhinolophidae); and a species of Nycteria, herein described tebrate hosts such as squamates, chelonians, birds, and mam- and named Nycteria heischi n. sp., from Megaderma spasma mals, including humans, in which five species of the genus Plasmodium are known to cause malaria (1, 2). The diversity of Significance Haemosporidia has been mostly investigated using mitochon- drial genes. In particular, the mitochondrial (mt) cytochrome Understanding the evolutionary history of Haemosporidian b (cytb) gene is one of the most widely used genetic markers to parasites would help to understand human malaria evolution. characterize the diversity of Haemosporidia parasites, and has Nevertheless, Haemosporidia parasite diversity in bats remains given rise to many phylogenetic reconstructions to document largely unstudied. In addition, some cases of unsuccessful PCR the evolutionary history of the Haemosporidia (3–5). All amplification of cytochrome b, the most widely used molecular Haemosporidia mt genomes previously sequenced share the marker to characterize Haemosporidia parasites, have recently same structure, characterized by a tandemly repeated linear el- been reported for Nycteria parasites infecting Nycteridae bats. ement of ∼6 kb containing the three protein-coding genes cytb, Here we used next-generation sequencing to characterize mi- cytochrome c oxidase subunit 1 (cox1), and cytochrome c oxidase tochondrial genomes of parasites from the Nycteria genus. Our subunit 3 (cox3) and two highly fragmented (small and large results have revealed an unsuspected mitochondrial genome subunits) ribosomal RNA (rRNA) genes (6). In the Plasmodium rearrangement within Haemosporidia. species, copy numbers of the mt genome are dozens to hundreds of times more numerous than the nuclear genomes (7, 8). Author contributions: I.L. and L.D. designed research; G.K., A.H., G.-C.G.T., I.L., and L.D. Consequently, mt genes are generally easily amplified using tra- performed research; A.H., G.-C.G.T., and L.D. collected blood from bats; G.K., A.H., B.S., F.A., F.J.A., I.L., and L.D. analyzed data; and G.K., A.H., B.S., F.A., F.J.A., I.L., and L.D. ditional PCR techniques. wrote the paper. Nevertheless, several cases of unsuccessful PCR amplification Reviewers: S.A., Yerevan State University; and G.S., UPMC Sorbonne Universités. of mt DNA markers have been recently reported, in particular for Nycteria and Plasmodium parasites infecting, respectively, The authors declare no conflict of interest. Nycteridae bats and Alaudidae birds (9, 10). Three alternative Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession nos. KX090645, KX090646, KX090647, and KX090648). hypotheses have been proposed to explain these negative results: 1 (i) loss of the mitochondrial genome during the evolution of these G.K. and A.H. contributed equally to this work. 2 parasites; (ii) transfer of some mitochondrial genes into the nu- Present address: Unité Biologie Moléculaire et Immunologie Parasitaire (UMR 956), Agence Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du clear genome; and (iii) technical problems due to the use of in- Travail–École Nationale Vétérinaire d’Alfort–Institut National de la Recherche Agrono- efficient or misdesigned primer sets. mique, 94701 Maisons-Alfort Cedex, France. Bats are hosts to a large, diverse, and specific array of 3To whom correspondence may be addressed. Email: [email protected] or [email protected]. Haemosporidia parasites (11). However, this parasite diversity This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. remains largely unstudied at the molecular and genomic levels, 1073/pnas.1610643113/-/DCSupplemental. 9834–9839 | PNAS | August 30, 2016 | vol. 113 | no. 35 www.pnas.org/cgi/doi/10.1073/pnas.1610643113 Downloaded by guest on September 25, 2021 EVOLUTION Fig. 1. Microphotographs of gametocytes of Nycteria parasites from N. grandis (A–H), M. spasma (I–L), and R. alycone (M–P). (A and B) Very young gametocytes. (C–E) Immature gametocytes. (F and G)Macro-andmicrogametocytes. (H) Old gametocyte of N. medusiformis from N. grandis (273VI). (I and J) Immature gametocytes. (K and L)Macro-andmicrogametocytesofN. heischi n. sp. from M. spasma (C289). (M and N) Immature gametocytes. (O and P) Macro- and microgametocytes of N. gabonensis from R. alcyone (289VI). (Scale bars, 1.5 μm.) (Megadermatidae). Our results have revealed an unsuspected irregularly scattered throughout the cytoplasm. Macrogametocytes mitochondrial genome rearrangement within the Haemosporidia. were highly chromophilic and appeared dark blue-purple with small and condensed nuclei. Microgametocytes had a pale pink Results color and the nuclei displayed a small central condensation of Three out of 13 N. grandis and four out of four R. alcyone from a chromatin reminiscent of a “cocarde” (rosette) (Fig. 1 A–H). The total of 195 bats (six families) were found to be infected with Nycteria sp. morphological type, observed in N. grandis in a Nycteria parasites in the Democratic Republic of Congo. Four mixed infection, was similar to N. medusiformis. Nevertheless, it out of five M. spasma from a total of 90 bats (six families) were did not present the highly characteristic filaments observed in found to be infected with Nycteria parasites in Cambodia. N. medusiformis. This morphotype differed mostly in size, in the All of the three N. grandis were coinfected with N. medusiformis nucleus of the microgametocytes, and in pigment features. (13) and an unidentified Nycteria sp. The four R. alcyone were in- However, the number of gametocytes of this Nycteria sp. was fected with N. gabonensis (14). N. medusiformis and N. gabonensis insufficient for a full description. N. medusiformis was highly were identified according to their morphological traits, from predominant, whereas Nycteria sp. was less frequent. N. grandis and R. alcyone,
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