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Identification of Cryptosporidium Bat Genotypes XVI–XVIII in Bats from Brazil

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Identification of Cryptosporidium Bat Genotypes XVI–XVIII in Bats from Brazil Parasitology Research (2019) 118:2183–2191 https://doi.org/10.1007/s00436-019-06342-6 GENETICS, EVOLUTION, AND PHYLOGENY - ORIGINAL PAPER Identification of Cryptosporidium bat genotypes XVI–XVIII in bats from Brazil Juliana Maria N. Batista1 & Cristiano de Carvalho1 & Wagner A. Pedro1 & Bruna N. Santana1 & Vinícius S. Camargo1 & Elis D. Ferrari1 & Isabela G. Nascimento1 & Marcelo V. Meireles1 Received: 6 November 2018 /Accepted: 29 April 2019 /Published online: 10 May 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Cryptosporidiosis is an emergent zoonotic disease caused by the globally distributed protozoa Cryptosporidium spp. Although several Cryptosporidium studies related to humans and many animal species have been published, there are still limited studies on the epidemiology of Cryptosporidium infection in bats. The aim of this study was to determine the occurrence of Cryptosporidium spp. and to perform the molecular characterization of Cryptosporidium species and genotypes in fecal samples from bats in an urban area of the municipality of Araçatuba, state of São Paulo, Brazil. Nested PCR targeting the 18S rRNA, actin, and HSP-70 genes was performed to screen 141 fecal samples from bats and detected Cryptosporidium spp. in 16.3% (23/141) of the samples. Bidirectional sequencing identified three novel Cryptosporidium bat genotypes (XVI, XVII, and XVIII) and a new genotype (18SH) genetically similar to Cryptosporidium avium in six species of bats. This is the first report on the occurrence and molecular characterization of Cryptosporidium spp. in Brazilian bats. Zoonotic Cryptosporidium species were not found in fecal samples from bats living in an urban area in the municipality of Araçatuba, state of São Paulo, Brazil. Keywords Chiropteran . Brazil . Cryptosporidial infection . Molecular characterization Introduction Although little information concerning the zoonotic potential of bat Cryptosporidium species or genotypes is available, bats may The order Chiroptera is the second most diverse among mam- be potential reservoirs of zoonotic microorganisms (Allocati et al. malian orders, with 1198 species described worldwide (Kasso 2016), including Cryptosporidium parvum and Cryptosporidium and Balakrishnan 2013;IUCN2018). In Brazil, Bordignon hominis (Kváč et al. 2015; Schiller et al. 2016). et al. (2017) reported the occurrence of 180 bat species. Bats Currently, there are nearly 38 Cryptosporidium species act as pollinators and seed dispersers of hundreds of plant classified in amphibians, birds, fishes, mammals, and reptiles. species (Bredt et al. 2012), and insectivorous bats play an In addition, several Cryptosporidium genotypes have been important role as insect predators (Peracchi et al. 2011). described based on molecular analyses (Feng et al. 2018). Cryptosporidial infection has been reported in humans and in Epidemiological studies performed up to date show a great domestic and wild animals, mainly as clinical or subclinical in- genetic diversity of the genus Cryptosporidium in bats and fections in the gastrointestinal tract (Santín 2012). Human infec- describe 15 Cryptosporidium genotypes in 12 species of bats tions with several Cryptosporidium species and genotypes have (Wang et al. 2013;Kváč et al. 2015; Murakoshi et al. 2016; also been reported as zoonotic and originated from domestic and Schiller et al. 2016; Murakoshi et al. 2018;Lietal.2019). wild animals (Chalmers and Giles 2010;Ryanetal.2016). The literature on taxonomy and the prevalence of cryptosporidial infection in chiropteran is scarce. In addition, Section Editor: Lihua Xiao there is no information on the clinicopathological features of Cryptosporidium infection in bats. Reports on the occurrence * Marcelo V. Meireles of Cryptosporidium sp. in fecal samples of bats were first [email protected] performed by Dubey et al. (1998), Morgan et al. (1998), Morgan et al. (1999), and Ziegler et al. (2007); however, 1 Faculdade de Medicina Veterinária, Universidade Estadual Paulista (UNESP), Araçatuba, Clóvis Pestana St., 793, 16050-680, Cryptosporidium species or genotypes were not determined Araçatuba, São Paulo, Brazil in these reports. 2184 Parasitol Res (2019) 118:2183–2191 The first description of the genetic characterization of bat Tween 20, sieved using a disposable plastic sieve, and centri- Cryptosporidium isolates was performed in China (Wang et al. fuged at 10.000g for 5 min. Fecal sediments were frozen at − 2013), with the designation of bat genotypes I and II in a 20 °C for DNA extraction and amplification by nested PCR. Chinese rufous horseshoe bat (Rhinolophus sinicus)and Stoliczka’s trident bat (Aselliscus stoliczkanus), respectively. Molecular characterization Kvác et al. (2015) described, in the USA and Czech Republic, bat genotype III in a large brown bat (Eptesicus fuscus)and The extraction of DNA was performed using the ZR Fecal bat genotype IV in a common pipistrelle (Pipistrellus DNA MiniPrep™ (Zymo Research) following the manufac- pipistrellus). In the Philippines, Murakoshi et al. (2016)de- turer’s guidelines. scribed bat genotype II in a Leschenault’srousette(Rousettus Three nested PCR protocols were performed to amplify leschenaultia) and greater musky fruit bat (Ptenochirus fragments of the actin (Sulaiman et al. 2002), 18S rRNA jagori), bat genotype V in a cave nectar bat (Eonycteris (Xiao et al. 2000), and HSP-70 (Morgan et al. 2001)genes, spelaea), bat genotype VI in a lesser short-nosed fruit bat following the author’s protocols, using the JumpStart™ Taq (Cynopterus brachyotis), and bat genotype VII in a ReadyMix™ (Sigma-Aldrich). As positive and negative con- Philippine forest horseshoe bat (Rhinolophus inops). Schiller trols, genomic DNA of C. parvum and ultrapure water were et al. (2016) described bat genotypes VIII, IX, X, and XI in used, respectively. The amplified fragments were subjected to gray-headed flying fox (Pteropus poliocephalus)inAustralia, electrophoresis on 1.5% agarose stained with GelRed™ and bat genotype XII was described in a northern bat (Biotium) and purified using the PureLink™ PCR (Eptesicus nilssonii) (Murakoshi et al. 2018) in Japan. The Purification Kit (Thermo Fisher Scientific) or the Illustra most recent study related to bat Cryptosporidium (Li et al. ExoProStar 1-Step™ (GE Healthcare Life Sciences). 2019) designated two genotypes identified in straw-colored Molecular cloning was performed when nested PCRs re- fruit bats (Eidolon helvum) from Nigeria as bat genotypes sulted in a low DNA yield, viewed as faint DNA bands by XIV and XV. Li et al. (2019) have also designated bat geno- electrophoresis, using the CloneJET™ PCR Cloning Kit fol- type XIII in substitution with bat genotype II (LC089978) lowing the manufacturer’s instructions (Thermo Fisher previously described by Murakoshi et al. (2016). Scientific). Plasmid DNA was purified with the GenElute™ The present study aimed to detect and perform the molec- Five-Minute Plasmid Miniprep Kit (Sigma-Aldrich). ular characterization of Cryptosporidium spp. in fecal samples from bats in an urban area of the municipality of Araçatuba, DNA sequence analysis state of São Paulo, Brazil. Genetic sequencing was performed using the ABI Prism™ Dye Terminator Cycling Sequence kit (Applied Biosystems) in an Materials and methods Automatic Sequencer ABI 3730XL (Applied Biosystems). DNA sequences were assembled with Codoncode Aligner Fecal samples version 7.1.1 software (CodonCode Corporation). The homol- ogy of amplified products to sequences from GenBank was This study was authorized by the Ethics Committee on assessed using BLAST (https://blast.ncbi.nlm.nih.gov/Blast. Animal Use (CEUA) of the São Paulo State University cgi) searches. Homologous sequences were aligned with (UNESP), School of Veterinary Medicine, Araçatuba, process consensus sequences using Clustal W (Thompson et al. no. 00507-2016. The capture of bats was authorized by the 1997) and BioEdit Sequence Alignment Editor (Hall 1999). Brazilian Institute for the Environment and Renewable Phylogenetic analyses were conducted in MEGA7 Natural Resources (IBAMA), permanent license no. 27346-1. (Kumar et al. 2016) using maximum likelihood analysis Bats were captured in forest fragments in an urban area in based on the Tamura 3-parameter model (Tamura 1992) the city of Araçatuba, state of São Paulo, Brazil, using fog and the general time reversible model (Nei and Kumar networks armed through vegetation at dusk. The captured bats 2000) for 18S rRNA and actin genes, respectively. Initial were placed in cotton bags (one for each bat) for approximate- tree(s) for the heuristic search were obtained automatically ly 60 min, and the bat species were then identified by mor- by applying neighbor-join and BioNJ algorithms to a matrix phological characteristics. The fecal samples excreted inside of pairwise distances estimated using the maximum com- the cotton bags were collected. The bats were released at the posite likelihood (MCL) approach and then selecting the same site of capture. topology with superior log-likelihood value. Substitution Each fecal sample was collected using a disposable wood- models and optional parameter sets were chosen using the en spatula, transferred to a 2-mL microtube, and stored at model selection option in MEGA7. Trees were rooted with 4 °C. Samples were fragmented and homogenized in a 2-mL sequences from Plasmodium falciparum JQ627151 and microtube containing phosphate-buffered saline and 0.1% EF472536 for 18S rRNA and actin genes, respectively.
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