Detection of Latino Virus (Arenaviridae Mammarenavirus
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Acta Tropica 179 (2018) 17–24 Contents lists available at ScienceDirect Acta Tropica journal homepage: www.elsevier.com/locate/actatropica Detection of Latino virus (Arenaviridae: Mammarenavirus) naturally T infecting Calomys callidus ⁎ Jorlan Fernandesa, , Renata Carvalho de Oliveiraa, Alexandro Guterresa, Débora Ferreira Barreto-Vieirab, Ana Claudia Pereira Terçasc, Bernardo Rodrigues Teixeirad, Marcos Alexandre Nunes da Silvab, Gabriela Cardoso Caldasb, Janice Mery Chicarino de Oliveira Coelhoe, Ortrud Monika Barthb, Paulo Sergio D’Andread, ⁎ Cibele Rodrigues Bonvicinod,f, Elba Regina Sampaio de Lemosa, a Laboratório de Hantaviroses e Rickettsioses, Fundação Oswaldo Cruz, Instituto Oswaldo Cruz, Rio de Janeiro, CEP 21040-360 RJ, Brazil b Laboratório de Morfologia e Morfogênese Viral, Fundação Oswaldo Cruz, Instituto Oswaldo Cruz, Rio de Janeiro, CEP 21040-360 RJ, Brazil c Universidade Estadual do Mato Grosso − UNEMAT, Tangará da Serra, CEP 78300-000 MT, Brazil d Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Fundação Oswaldo Cruz, Instituto Oswaldo Cruz, Rio de Janeiro, CEP 21040-360 RJ, Brazil e Laboratório de Anatomia Patológica, Fundação Oswaldo Cruz, Instituto Nacional de Infectologia Evandro Chagas, Rio de Janeiro, CEP 21040-360 RJ, Brazil f Instituto Nacional do Câncer – INCA, Rio de Janeiro, CEP 20230-092 RJ, Brazil ARTICLE INFO ABSTRACT Keywords: Mammarenavirus species are associated with a specific rodent host species, although an increasing number of Arenavirus virus has been associated to more than one host, suggesting that co-evolution is less robust than initially thought. Mammarenavirus There are few eco-epidemiological studies of South America mammarenaviruses in non-endemic areas of Rodent Arenavirus Hemorrhagic Fever, affecting specially our current knowledge about animal reservoirs and virus Calomys callidus range and host-virus relations. In Brazil, seven arenavirus species were described in seven different rodent Latino virus species. Here in we describe a new rodent reservoir species in Brazil related to the previously described Latino mammarenavirus (LATV) MARU strain. Samples of 148 rodents from Mato Grosso state, Brazil were analyzed. Amplification of the glycoprotein precursor gene (GPC) was observed in six Calomys callidus rodents. According to phylogenetic inferences, is observed a well-supported monophyletic clade of LATV from C. callidus and other Clade C mammarenavirus. In addition, the phylogenetic relations of both genes showed a close relation between LATV MARU and Capão Seco strains, two distinct lineages. Additionally, the results obtained in this study point out to a change of scenario and in previously stabilized patterns in the dynamics of South American mam- marenaviruses, showing that with more studies in AHF non-endemic or silent areas, more potential hosts for this virus will be discovered. 1. Introduction are divided in two main groups: the Old world (Lassa − Lymphocytic choriomeningitis virus serocomplex) and the four New World (Tacaribe Arenaviruses are zoonotic agents associated mainly to small mam- serocomplex) lineages, designated A, B, C and A recombinant (Emonet mals (Charrel and de Lamballerie, 2010). In the last few years, changes et al., 2009; Radoshitzky et al., 2015). have been made to the family Arenaviridae driven by the detection of Although each mammarenavirus specie is usually associated with a divergent arenavirus in boid snakes. The current taxonomic status by specific rodent host species (Salazar-Bravo et al., 2002), an increasing ICTV divides the Arenaviridade family in two: Mammarenavirus and number of virus has been associated to more than one host (Lavergne Reptarenavirus, from mammalian and reptile hosts, respectively et al., 2015; Milazzo et al., 2011, 2015). For example, Lassa virus (Radoshitzky et al., 2015). Mammareanaviruses are composed by harbored by Mastomys natalensis, is also hosted by other rodent species, highly divergent rodent born viruses, except for Tacaribe virus isolated Hylomyscus pamfi and Mastomys erythroleucus,indifferent geographic from fruit bats and ticks (Downs et al., 1963; Sayler et al., 2014), and regions from Africa (Olayemi et al., 2016). These findings alongside the ⁎ Corresponding authors. E-mail addresses: jorlan@ioc.fiocruz.br (J. Fernandes), elemos@ioc.fiocruz.br (E.R.S. de Lemos). https://doi.org/10.1016/j.actatropica.2017.12.003 Received 4 October 2017; Received in revised form 27 November 2017; Accepted 2 December 2017 Available online 05 December 2017 0001-706X/ © 2017 Elsevier B.V. All rights reserved. J. Fernandes et al. Acta Tropica 179 (2018) 17–24 recent discovery of reptarenaviruses and more depth analyses of Bionomic and biometric data were collected, and specimens were mammarenavirus relations, suggest that co-evolution is less robust than identified at specific level by both karyotyping and cranial mor- initially thought (Blasdell et al., 2016; Irwin et al., 2012; Zapata and phology/morphometry and confirmed by amplification of the cyto- Salvato, 2013). chrome b gene (Bonvicino et al., 1996, 2002). In addition, there are few eco-epidemiological studies of South All procedures using animals as described in this manuscript were America mammarenaviruses in non-endemic areas of Arenavirus conducted in accordance with the standard operating protocols ap- Hemorrhagic Fever (AHF), affecting specially our current knowledge proved by the Animal Ethics Committee of the Instituto Oswaldo Cruz about animal’s reservoirs and virus range and host-virus relations. − FIOCRUZ and by the Chico Mendes Institute for the Biodiversity Herein we describe a new rodent reservoir, Calomys callidus, detected in Conservation (ICMBio). Brazil and related to a known lineage of Latino mammarenavirus from Bolivia. 2.2. Mammarenavirus detection 2. Materials and methods The genomic RNA was obtained from spleen and liver tissue samples ® according to the manufactureŕs instructions from the PureLink Micro- 2.1. Small-mammals trapping to-Midi total RNA purification kit (Invitrogen, San Diego, CA, USA). The amplification process was performed according to previously described Rodents were captured using live traps during fieldworks in protocols (Bowen et al., 1996b; García et al., 2000). In addition, viral September and December 2010–Sapezal (13°32′33” S/58°48′51” W) RNA was also extracted from lung, kidney and heart from positive ro- and Comodoro (13°39′46” S/59°47′09” W) municipalities − and March dent samples. 2015 − Campo Novo do Parecis (13°40′31” S/57°53′31” W) and Tangará da Serra (14° 37′ 08” S/57° 29′ 09” W) municipalities, in Mato 2.3. DNA sequencing and phylogenetic analyses Grosso state, Brazil (Fig. 1). ® Blood and tissue samples from the wild rodents were obtained in For DNA purification, the Wizard SV Gel and PCR Clean-Up System accordance with recommended safety procedures (de Lemos and kit (Promega, Corp., Madison, WI, USA) was used according to the D’Andrea, 2014), after authorization by the Chico Mendes Institute for manufacturer’s recommendations and strands were directly sequenced. ® the Biodiversity Conservation (ICMBio) under license number 13373. BigDye Terminator™ version 3.1 Cycle Sequencing Kit (Applied Fig. 1. Geographic distribution of Calomys callidus (dark gray area) and Calomys callosus (light gray area) highlighting central-western region of Brazil, showing the municipalities of Comodoro, Sapezal, Campo Novo do Paresis and Tangará da Serra (▲1,2,3 and 4, respectively). Circles (●) = Latino mammarenavirus (LATV) detection in Brazil (Fernandes et al., 2015). Squares (■) = LATV detection in Bolivia (Cajimat et al., 2009). 18 J. Fernandes et al. Acta Tropica 179 (2018) 17–24 Fig. 2. Phylogenetic trees based on the GPC protein (323 aa) sequences of mammarenaviruses, using ML and Bayesian methods. Numbers (> 0.7/ > 70%) above branches indicate posterior node probabilities or bootstrap values (MrBayes/ML). *Indicate values below 0.7/70. †Exhibited difference between ML and MrBayes tree-building method topology. Gray indicates New World Clade C Mammarenavirus. Abbreviations: C. callidus (=Calomys callidus), C. callosus (=Calomys callosus), N. lasiurus (=Necromys lasiurus), MT (=Mato Grosso) and MS (=Mato Grosso do Sul). Biosystems) in an automatic sequencer (Applied Biosystems, ABI PRISM selection to be integrated across all best-fit models. The MCMC settings 3130X model, Foster City, CA, USA). Nucleotide sequences were ana- consisted of two simultaneous independent runs with 4 chains each that lyzed using MEGA7 software (Kumar et al., 2016), and a consensus were run for 10 million generations and sampled every 100th genera- sequence was derived from contiguous assembled with the same soft- tion, yielding 100,000 trees. After eliminating 10% of the samples as ware. burn-in, a consensus tree was built. Statistical support of the clades was Multiple sequence alignment and comparison of amino acid were measured by a heuristic search with 1000 bootstrap replicates and the performed using MAFFT version 7 employing the E-INS-i algorithm, in Bayesian posterior probabilities. The best-fit evolutionary model was the Jalview v.4 software program (Waterhouse et al., 2009). Phyloge- determined using MEGA version 7, using the Bayesian Information netic relationships were estimated using (a) Maximum likelihood (ML) Criterion (Kumar et al., 2016). Sequences used in the phylogenetic phylogenetic inference using PhyML implemented in SeaView v.4 analyses are listed on Supplementary Table 1. software program (Gouy et al.,