A Rickettsia parkeri-like agent infecting Amblyomma calcaratum nymphs from wild birds in Mato Grosso do Sul, Brazil

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Author's personal copy Ticks and Tick-borne Diseases 4 (2013) 145–147

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A Rickettsia parkeri-like agent infecting Amblyomma calcaratum nymphs from wild birds in Mato Grosso do Sul, Brazil Maria Ogrzewalska a , Thiago Martins a , Miroslav Capek b , Ivan Literak c,d,∗ , Marcelo B. Labruna a a

Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootecnia, Universidade de São Paulo, São Paulo, Brazil Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v. v. i., Brno, Czech Republic c Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic d CEITEC VFU, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic b

a r t i c l e

i n f o

Article history: Received 7 March 2012 Received in revised form 3 July 2012 Accepted 3 July 2012 Keywords: Rickettsia Amblyomma Birds Brazil

a b s t r a c t In total, 142 birds, mostly passerines, belonging to 42 species were examined for the presence of ticks in 3 locations in Mato Grosso do Sul Brazil during 2006. Seven birds (5%) were infested with 4 nymphs of Amblyomma calcaratum (Ramphocelus carbo, 3 infested/12 examined) and 5 larvae of Amblyomma sp. (Furnarius rufus, 2/5; Turdus leucomelas, 1/6; and Paroaria capitata, 1/8). All 4 nymphs of A. calcaratum tested by polymerase chain reaction targeting rickettsial genes gltA and ompA and by amplicon sequencing were found to be infected with a Rickettsia sp. strain NOD, a Rickettsia parkeri-like agent. A. calcaratum infected with a rickettsial bacterium was found for the first time. © 2012 Elsevier GmbH. All rights reserved.

Introduction Ticks in Brazil comprise 64 species, among which 44 and 20 belong to the families Ixodidae and Argasidae, respectively (DantasTorres et al., 2009, 2012; Labruna and Venzal, 2009; Nava et al., 2010). The ixodid genus Amblyomma is the most numerous with 29 well-established species (Martins et al., 2010). Knowledge of these ticks is mostly restricted to a list of known hosts for the adult individuals, and there is a lack of information about their immature stages, biology or role in the transmission of pathogens. While adult Amblyomma calcaratum (Neumann, 1899) are known to parasitize mainly anteaters (Aragao, 1936; Jones et al., 1972; Guglielmone et al., 2003); a few studies have suggested that A. calcaratum larvae and nymphs feed preferably on birds (Jones et al., 1972; Labruna et al., 2007; Ogrzewalska et al., 2009b, 2010, 2011). To date, no microorganism has been reported to infect A. calcaratum. Bacteria of the genus Rickettsia are obligate intracellular organisms that infect invertebrate hosts worldwide (Raoult and Roux, 1997). In South America, the most important tick-borne zoonotic disease is Rocky Mountain spotted fever (RMSF), which is caused by the bacterium Rickettsia rickettsii (Labruna, 2009). In recent years,

∗ Corresponding author at: Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Palackeho 1-3, 612 42 Brno, Czech Republic. E-mail address: [email protected] (I. Literak). 1877-959X/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.ttbdis.2012.07.001

however, at least 7 other tick-associated Rickettsia species have been reported from this continent (Labruna et al., 2011). We present here the first record of the tick A. calcaratum infected with a R. parkeri-like agent, which was found on wild birds in Brazil. Materials and methods Ticks were collected from birds in the state of Mato Grosso do Sul, West Central Brazil, during July–August 2006. Birds were trapped using mist nets placed in fragmented habitats within the Cerrado biome, a kind of woodland savanna which formerly dominated the Central Brazilian Plateau. Each individual bird was identified using Sigrist (2004) and examined visually for the presence of ticks. Ticks were collected using tweezers and placed into tubes with 70% ethanol. After processing, captured birds were released back into the wild as quickly as possible to minimize the disturbance. The study locations were as follows: Nova Andradina (22◦ 15′ S, 53◦ 21′ W; birds were examined during 16–17 and 29–30 July, and 10–11 August 2006), Margarida at the foothills of the Cerra de Bodoquena (21◦ 30′ S, 56◦ 40′ W; 20–22 July 2006), and Ivinhema River (22◦ 31′ S, 53◦ 30′ W, 12 and 15 August 2006). Ticks were identified morphologically to the genus level following Barros-Battesti et al. (2006), whereas Amblyomma nymphs were identified based on the study by Martins et al. (2010). Ticks were tested individually for the presence of Rickettsia by polymerase chain reaction (PCR) using primers CS-78 (5′ -GCA AGT ATC GGT GAG GAT GTA AT-3′ ) and CS-323 (5′ -GCT TCC TTA AAA TTC AAT AAA TCA GGA T-3′ ) targeting a 401-bp fragment of the rickettsial

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Table 1 List of birds captured with Amblyomma ticks in Mato Grosso do Sul, Brazil during 2006. Birds


Species (order, family)

No. infested/no. captured (%)




Furnarius rufus (Passeriformes, Furnariidae) Turdus leucomelas (Passeriformes, Turdidae) Ramphocelus carbo (Passeriformes, Thraupidae) Paroaria capitata (Passeriformes, Thraupidae)

2/5 (40) 1/6 (17) 3/12 (25) 1/8 (13)

Amblyomma sp. Amblyomma sp. A. calcaratum Amblyomma sp.

2 larvae 2 larvae 4 nymphs 1 larva

Nova Andradina Nova Andradina Ivinhema River Ivinhema River

gene gltA that occurs in all Rickettsia species (Labruna et al., 2004) and primers Rr190.70 (5′ -ATG GCG AAT ATT TCT CCA AAA-3′ ) and Rr190.701 (5′ -GTT CCG TTA ATG GCA GCA TCT-3′ ) targeting a 617bp fragment of the ompA gene present only in Rickettsia species belonging to the spotted fever group (SFG) (Regnery et al., 1991). PCR products were DNA-sequenced and analyzed in BLAST to determine similarities to other Rickettsia species (Altschul et al., 1990).

Results In total, 142 birds, mostly passerines, belonging to 42 species were examined. Seven birds (5%) were infested with ticks (Table 1). No ticks were found on the following bird species (number of individuals in parentheses): Agelaioides badius (2), Colaptes melanochloros (2), Columbina picui (6), Columbina squammata (9), Columbina talpacoti (5), Coryphospingus cucullatus (2), Crotophaga ani (3), Dryocopus lineatus (1), Euphonia chlorotica (1), Falco sparverius (2), Formicivora rufa (2), Glaucidium brasilianum (3), Hemitriccus obsoletus (1), Chlorostilbon aureoventris (2), Lepidocolaptes angustirostris (1), Leptotila verreauxi (1), Megascops choliba (1), Mimus saturninus (1), Molothrus bonariensis (12), Myiarchus ferox (1), Myiarchus swainsoni (1), Myiarchus tyrannulus (2), Myiophobus fasciatus (1), Nandayus nenday (1), Passer domesticus (1), Pitangus sulphuratus (6), Phacellodomus rufifrons (7), Phaethornis pretrei (2), Poospiza melanoleuca (1), Progne chalybea (2), Sicalis flaveola (1), Sublegatus modestus (1), Tachyphonus rufus (1), Tangara cayana (7), Thraupis sayaca (3), Troglodytes musculus (6), and Volatinia jacarina (1). Both rickettsial genes gltA and ompA were proven by PCR in all 4 nymphs of A. calcaratum found on 3 individuals of Ramphocelus carbo near Ivinhema River. The gltA PCR amplicons from positive ticks were sequenced and found to be identical to one another. These sequences were identical (100%, 331/331 bp) to the corresponding sequence of R. parkeri strain At24 (EF102236) isolated from A. triste ticks in Brazil (Silveira et al., 2007), Rickettsia sp. strain Atlantic rainforest (GQ855235) recently reported as the etiological agent of clinical cases of SFG rickettsiosis in Brazil (Spolidorio et al., 2010; Silva et al., 2011), Rickettsia sp. strain NOD (EU567177) isolated from A. nodosum ticks in Brazil (Ogrzewalska et al., 2009a), Rickettsia sp. strain ApPR (GenBank accession number JN126320) from A. parkeri ticks in Brazil (Pacheco et al., 2012), and Rickettsia sp. strain COOPERI (AY362704) isolated from A. dubitatum ticks in Brazil (Labruna et al., 2004) as well as with R. sibirica (RSU59734), and R. africae (HQ335126). The ompA PCR amplicons of the nymphs were identical (100%, 491/491 bp) to the corresponding sequence of the Rickettsia sp. strain NOD (EU567180) isolated from A. nodosum ticks in Brazil (Ogrzewalska et al., 2009a), and 98.6% (484/491) similar to Rickettsia sp. strain ApPR from southern Brazil (JN126318) (Pacheco et al., 2012), 98.4% (483/491 bp) identical to Rickettsia sp. strain Cooperi (AY362706), 97.8% (453/463) identical to Rickettsia sp. strain Atlantic rainforest (GQ855237), and 97.6% (576/590 bp) identical to R. africae (CP001612). No rickettsial DNA was determined in larvae of Amblyomma sp. found on Furnarius rufus, Turdus leucomelas, and Paroaria capitata.

Discussion A. calcaratum has been reported to occur in a number of countries in Central and South America (Caceres et al., 2002; Guglielmone et al., 2003). Recently, it was found in Mexico (Guzman-Cornejo et al., 2006). There is also one isolated record of an adult A. calcaratum in the U.S.A., which seemed to be the result of rare transportation of an engorged nymph via a migratory bird (Bloemer et al., 1987). In Brazil, A. calcaratum has a widespread distribution, encompassing all major regions (Aragao, 1936; Arzua et al., 2005; Botelho et al., 1989; Brum et al., 2003; Cutolo et al., 2000; Evans et al., 2000; Labruna et al., 2005, 2007; Martins and Guglielmone, 1995; Ogrzewalska et al., 2009b, 2010, 2011; Pacheco et al., 2012; Robinson, 1926). The adult stage parasitizes chiefly the anteaters Tamandua spp. and Myrmecophaga tridactyla. A few reports refer to immature stages parasitizing birds and adult stages parasitizing other mammal species, such as Procyon cancrivorus, Choloepus hoffmanni, and Mazama americana. Our study adds the bird Ramphocelus carbo as a new host for A. calcaratum. We found for the first time A. calcaratum infected with a rickettsial bacterium. DNA sequences of SFG rickettsiae generated from A. calcaratum nymphs indicate that these nymphs were infected with Rickettsia sp. strain NOD, since both gltA and ompA partial sequences were 100% identical between the A. calcaratum agent (present study) and the strain NOD (Ogrzewalska et al., 2009a). Previous studies have considered strain NOD as well as other South American rickettsial strains (Cooperi, Atlantic rainforest, and ApPR) to represent different strains of R. parkeri, which are very closelyrelated to R. africae and R. sibirica (Medeiros et al., 2011; Pacheco et al., 2012). In fact, it has been suggested by phylogenetic analyses that R. parkeri, R. africae, R. sibirica, and other South American R. parkeri-like strains represent a single Rickettsia species (Pacheco et al., 2012). Until this issue is resolved, we consider strain NOD to be a R. parkeri-like agent. Strain NOD has been reported infecting immature stages of A. nodosum and A. longirostre ticks collected from birds in the states of São Paulo (southeastern Brazil) and Parana (southern Brazil), respectively (Ogrzewalska et al., 2009a; Pacheco et al., 2012). Both these states border the state of Mato Grosso do Sul. Other R. parkerilike agents, R. parkeri strain At24 and R. parkeri strain Maculatum 20 have been reported infecting Amblyomma spp. ticks in Brazil (Labruna et al., 2004; Medeiros et al., 2011; Pacheco et al., 2012; Sabatini et al., 2010; Silveira et al., 2007). At least 2 of these agents, namely the Maculatum 20 strain from A. triste (Silveira et al., 2007) and the Atlantic rainforest strain from A. ovale and A. aureolatum (Medeiros et al., 2011; Sabatini et al., 2010), were recently proven to cause spotted fever in humans in South America (Romer et al., 2011; Spolidorio et al., 2010). Therefore, the remaining strains of R. parkeri-like agents, including the NOD strain, should be regarded as potential human pathogens. Neither A. calcaratum nor A. nodosum have ever been reported to bite humans, whereas A. longirostre has been reported to infest humans, but only sporadically (Guglielmone et al., 2006; SerraFreire, 2010). Even though the chances for these 3 tick species to transmit strain NOD to humans is presumed to be quite low, the fact that the strain NOD was found to infect 3 different tick species

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