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Rickettsia Species in Ticks That Parasitize Amphibians and Reptiles

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Rickettsia Species in Ticks That Parasitize Amphibians and Reptiles Ticks and Tick-borne Diseases 10 (2019) 987–994 Contents lists available at ScienceDirect Ticks and Tick-borne Diseases journal homepage: www.elsevier.com/locate/ttbdis Original article Rickettsia species in ticks that parasitize amphibians and reptiles: Novel T report from Mexico and review of the worldwide record Sokani Sánchez-Montesa, Ana Belem Isaak-Delgadob, Carmen Guzmán-Cornejoc, Emilio Rendón-Francod, Claudia I. Muñoz-Garcíad, Sergio Bermúdeze, Jorge Morales-Diazf, Anabel Cruz-Romerof, Dora Romero-Salasf, Karla Dzul-Rosadog, César Lugo-Caballerog, ⁎ Pablo Colunga-Salasa, Ingeborg Beckera, a Centro de Medicina Tropical, Unidad de Investigación en Medicina Experimental, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad de México, Mexico b Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Ciudad de México, Mexico c Laboratorio de Acarología, Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico d Departamento de Producción Agrícola y Animal, Universidad Autónoma Metropolitana Unidad Xochimilco, Ciudad de México, Mexico e Departamento de Investigación en Entomología Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama f Facultad de Medicina Veterinaria y Zootecnia, Región Veracruz. Universidad Veracruzana, Mexico g Centro de Investigaciones Regionales “Dr. Hideyo Noguchi”, Universidad Autónoma de Yucatán, Yucatán, Mexico ARTICLE INFO ABSTRACT Keywords: Ticks are obligate haematophagous ectoparasites that are associated with a wide range of vertebrate hosts, Rickettsia species among them also reptiles and amphibians. They have dynamic ecological interactions with multiple micro- Amblyomma dissimile organisms, ranging from endosymbionts to pathogens, such as the members of the genus Rickettsia. The aim of Amblyomma mixtum this work was to detect Rickettsia in ticks from amphibians and reptiles from southern Mexico by the amplifi- Reptile cation, sequencing and phylogenetic reconstruction of the gltA and ompA genes, and also to compile all the Amphibians published records worldwide of Rickettsia associated with ticks attached to reptiles and amphibians, in order to Mexico elucidate the host-parasite relationships, and to identify the geographical distribution of each bacterial species. We record for the first time the presence of Rickettsia sp. strain Colombianensi and Rickettsia amblyommatis in ticks from several reptiles and amphibians collected in three new localities from the states of Guerrero and Veracruz, Mexico. Additionally, we here report 23 Rickettsia taxa associated with 18 tick species attached to 42 host taxa of amphibians and reptiles in 36 countries. Our findings increase the inventory of rickettsia reported in Mexico and summarizes the knowledge of these bacteria associated with ticks of this particular group of ver- tebrate host worldwide. 1. Introduction (Smyth, 1973; Guglielmone and Nava, 2010). There are other tick species that are considered parasites of mammals or birds, yet they can Ticks are obligate haematophagous ectoparasites that are associated also parasitize exceptionally reptiles or amphibians when their natural with a wide range of vertebrate hosts. More than 900 species are re- hosts are not available (e.g. Amblyomma mixtum or Amblyomma macu- cognized worldwide (210 soft ticks, 707 hard ticks), with a significant latum). In this case however, it is not known whether the change of the increase in recent years of the species described from amphibians and host also benefits these species (Estrada-Peña et al., 2005; Nava et al., reptiles (Guglielmone et al., 2014; Barros-Battesti et al., 2015; Muñoz- 2014; Guglielmonne et al. 2014). Leal et al., 2016a, 2017). Some tick species have established very close Ticks also have dynamic ecological interactions with multiple mi- relationships with these vertebrate groups, with a marked preference croorganisms, ranging from endosymbionts to pathogens. A well-stu- for amphibians and reptiles, such as Amblyomma rotundatum in the died group of microorganisms associated with ticks are the members of Neotropical region or Bothriocroton hydrosauri in the Australian region the genus Rickettsia. These taxa encompass 30 obligate intracellular ⁎ Corresponding author at: Centro de Medicina Tropical, Unidad de Investigación en Medicina Experimental, Facultad de Medicina, Universidad Nacional Autónoma de México, C.P. 04510, Ciudad de México, Mexico. E-mail address: [email protected] (I. Becker). https://doi.org/10.1016/j.ttbdis.2019.04.013 Received 27 June 2018; Received in revised form 15 April 2019; Accepted 16 April 2019 Available online 17 April 2019 1877-959X/ © 2019 Elsevier GmbH. All rights reserved. S. Sánchez-Montes, et al. Ticks and Tick-borne Diseases 10 (2019) 987–994 Table 1 Sampling sites of specimens collected in this study. State Locality Geographic reference Collection date Guerrero Barra de Potosi (BP) 17.537400°-101.442137° 04-09 July, 2015 22 December, 2015 Tabasco La Florida (LF) 17.462759°-92.770590° 18 November, 2015 Villahermosa (VI) 18.006182°-92.931791° 31 July, 2016 Veracruz Cotaxtla (CO) 18.833333°-96.383333° 05 February, 2018 Veracruz Sontecomapan (SO) 18.490689°-95.064364° 18 May, 2018 Veracruz Veracruz (VE) 19.171486°-96.210503° 03 November, 2018 coccobacilli, with 15 pathogenic species that can cause acute diseases Raoult (2009) which are based on the degree of nucleotide identity of such as Rocky Mountain spotted fever and Rickettsia parkeri rickettsiosis the genes gltA (≥99.9%) and ompA (≥98.8) with the most homologous (Shpynov et al., 2018). validated species. In Mexico, eight tick species (two soft ticks [Ornithodoros talaje, In addition, we performed a phylogenetic reconstruction. For this Ornithodoros turicata] and six hard ticks [Amblyomma dissimile, A. reason, we performed global alignments using the Clustal W algorithm. mixtum, A. rotundatum, Amblyomma sabanerae, Amblyomma scutatum Subsequently, the best substitution model was selected, based on the and Robertsicus elaphense]) were found to be associated naturally with lowest value of the Bayesian Information Criterion (BIC). For Rickettsia one amphibian species (a toad) and 19 reptiles (seven lizard, six turtle, identification, we conducted a phylogenetic reconstruction using the three snake and three crocodylians species) (Paredes-León et al., 2008; Maximum Likelihood method (ML) with 10,000 bootstrap replications Guzmán-Cornejo et al., 2011; Charruau et al., 2016). Despite the above, using the close neighbor interchange method in the software Mega 7.0. the presence and diversity of Rickettsia associated with ticks of both Gaps were excluded from the analysis. vertebrate groups, particularly those species of wide distribution and Additionally, an extensive review of Rickettsia identified in ticks close to human settlements, have not been studied in Mexico. Fur- from reptiles and amphibians was made in specialized databases thermore, since the literature related to Rickettsia in ticks of amphibians (BioOne, Google Scholar, Highwire, Medline, Pubmed, Scielo, Scopus, and reptiles is very recent, and most of the studies have been conducted and Zoological Records), using several combinations of keywords: in South America (Muñoz-Leal et al., 2016b; Luz et al., 2018; “tick”, “tick borne-pathogen”, “tick borne-diseases”, “reptiles”, “am- Santodomingo et al., 2018), the aim of this work was to detect Rickettsia phibians” and “Rickettsia”. in ticks from amphibians and reptiles from southern Mexico, and to compile all the published records worldwide, in order to elucidate the 3. Results host-parasite relationships, and to identify the geographical distribution of each Rickettsia species. 3.1. New records in Mexico 2. Material and methods One hundred and sixty-five hard ticks were collected (163 A. dis- simile, and 2 A. mixtum) and screened for Rickettsia. All the larvae pools As a part of two ongoing projects aimed to identify the diversity of produced a single sequence of the 16S-rRNA gene, which exhibits an bacterial pathogens and ectoparasites in amphibians and reptiles, 23 identity of 100% with A. dissimile sequences deposited in GenBank hosts parasitized by ticks were enrolled in this study. They belonged to under accession KY389390.1. Twenty-two hosts of the three inspected the following species: Boa constrictor (common boa), Iguana iguana species were infested with A. dissimile, and a single I. iguana exhibited a (green iguana), and Rhinella marina (cane toad), and were captured in coinfestation of A. dissimile together with A. mixtum. Amplicons of the three coastal states of Mexico (Table 1). Animals were physically re- gltA gene corresponding to the expected size were detected in 14 ticks, strained, identified morphologically at species level using the taxo- of which one was a female A. mixtum and 13 were A. dissimile (1 male, 2 nomic keys of Stebbins (2003), visually inspected for ticks, and finally females, 5 nymphs, and 5 larvae) from six individual hosts of the three released in situ. Procedures were carried out under authorization of the species, where each tick was positive for a single Rickettsia species. The Secretaría del Medio Ambiente y Recursos Naturales (SEMARNAT), Blast analysis of the fragment of 760 bp fragment of the gltA gene of permit reference FAUT-0250. Amblyomma dissimile yielded an identity of 99.45% with Rickettsia Ticks were fixed in absolute ethanol, and identified using the monacensis strain IrR/Munich
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