Elsevier

Ticks and Tick-borne Diseases

Volume 7, Issue 6, October 2016, Pages 1089-1096
Ticks and Tick-borne Diseases

Original article
New Rickettsia species in soft ticks Ornithodoros hasei collected from bats in French Guiana

https://doi.org/10.1016/j.ttbdis.2016.09.004Get rights and content

Highlights

  • A novel Rickettsia was detected in Ornithodoros hasei ticks feeding on Noctilio albiventris bats.

  • Sequencing and phylogenetic analysis revealed that this novel Rickettsia species is genetically very close to Rickettsia peacockii.

  • This is the first report showing the presence of nucleic acid of Rickettsia sp. in Ornithodoros hasei ticks from South American bats.

  • Candidatus Rickettsia wissemanii is proposed to name this microorganism.

Abstract

In French Guiana, located on the northeastern coast of South America, bats of different species are very numerous. The infection of bats and their ticks with zoonotic bacteria, especially Rickettsia species, is so far unknown. In order to improve knowledge of these zoonotic pathogens in this French overseas department, the presence and diversity of tick-borne bacteria was investigated with molecular tools in bat ticks.

In the beginning of 2013, 32 bats were caught in Saint-Jean-du-Maroni, an area close to the coast of French Guiana, and the ticks of these animals were collected. A total of 354 larvae of Argasidae soft ticks (Ornithodoros hasei) from 12 bats (Noctilio albiventris) were collected and 107 of them were analysed. DNA was extracted from the samples and quantitative real-time PCR was carried out to detect Rickettsia spp., Bartonella spp., Borrelia spp. and Coxiella burnetii. All tested samples were negative for Bartonella spp., Borrelia spp. and Coxiella burnetii. Rickettsia DNA was detected in 31 (28.9%) ticks. An almost entire (1118 base pairs long) sequence of the gltA gene was obtained after the amplification of some positive samples on conventional PCR and sequencing. A Bayesian tree was constructed using concatenated rrs, gltA, ompA, ompB, and gene D sequences. The study of characteristic sequences shows that this Rickettsia species is very close (98.3–99.8%) genetically to R. peacockii. Nevertheless, the comparative analysis of sequences obtained from gltA, ompA, ompB, rrs and gene D fragments demonstrated that this Rickettsia is different from the other members of the spotted fever group. The sequences of this new species were deposited in GenBank as Candidatus Rickettsia wissemanii. This is the first report showing the presence of nucleic acid of Rickettsia in Ornithodoros hasei ticks from South American bats.

Introduction

Rickettsiae are obligate intracellular gram-negative bacteria transmitted by blood-feeding arthropods, primarily ticks, which may act as vectors, reservoirs, and/or amplifiers in the life cycles of the bacteria (Raoult and Roux, 1997). Ixodid ticks, also called hard ticks, are the main vectors of Rickettsiae (Parola et al., 2013). There are at least six genera (Rhipicephalus, Dermacentor, Amblyomma, Haemaphysalis, Hyalomma and Ixodes) which are recognized as competent vectors (Parola and Raoult, 2001). Concerning soft ticks (Argasidae), R. bellii is found in both Argas and Ornithodoros genera, and it is the most common Rickettsia found in ticks in United States of America (Raoult and Roux, 1997, Ogata et al., 2006). Recently described, the spotted fever group Rickettsia hoogstraalii is regularly identified in Ornithodoros spp. and Haemaphysalis spp. ticks (Duh et al., 2010, Dietrich et al., 2014). In humans, rickettsiae are the causative agents of the tick-borne rickettsioses, characterized by clinical features including fever, headache, rash, and occasional eschar formation at the site of the tick bite (Parola et al., 2013).

French Guiana is an overseas territory situated between Brazil and Suriname, and its size (84,000 km2) is equivalent to about one fifth of the territory of mainland France; it is a sparsely populated department. Its climate is equatorial (hot and humid) and the Amazon rainforest covers 90% of its territory. Its ecosystem is characterized by a rich fauna and flora (5500 species of plants, 700 species of birds, and 177 species of mammals) and a dense river network. To our knowledge, in French Guiana only one Rickettsia, Candidatus R. amblyommii, has been detected in Amblyomma coelebs ticks (Parola et al., 2007). This rickettsia, with unknown pathogenic potential, is very common in North and Central America (Parola et al., 2013).

In French Guiana, bats of different species are very numerous. It is estimated that there are approximately 110 species. The infection of bats and their ticks with bacterial pathogens such as Rickettsia spp., Bartonella spp., Borrelia spp. and Coxiella burnetii is so far unknown. In order to improve the knowledge of these zoonotic pathogens in this country, the presence and diversity of these tick-transmitted pathogens were investigated with molecular tools in bat ticks.

Section snippets

Study site and bat samples

In January 2013, 32 bats (Chiroptera) were caught in Saint-Jean-du-Maroni (05°23′95″N–54°04′72″W), an area close to the coast of French Guiana, and the ticks (N = 354) of these animals were collected. Bats were caught with mist nets. Catches occurred in unoccupied buildings. The identification of bats was performed using previously described conventional morphological keys (Brosset and Charles-Dominique, 1990).

Collection and identification of ticks

A total of 32 apparently healthy bats were captured; species and sex were identified.

Tick identification

In the location of Saint Jean du Maroni, a total of 32 bats belonging to Noctilio albiventris (Fig. 1) were captured and examined; 12 (37.5%) of them (8 males and 4 females) were found to be infested with soft tick larvae. The bats’ infestation varied between 4 and 67 ticks per specimen, with an average infestation of 29.5 ± 21. During this study, a total of 354 tick larvae were collected (Table 1). Of these, 16 ticks were randomly selected and identified with molecular tools as Ornithodoros hasei

Discussion

In French Guiana, bats are very numerous, with a great diversity of species. The order Chiroptera comprises more than 100 species. Bats represent 54% of the total number of wild animal species (Charles-Dominique et al., 2001). The lesser bulldog bat (Noctilio albiventris) is an insectivorous and occasionally carnivorous bat of the Neotropic ecozone. Its distribution range extends from southern Mexico to eastern Brazil, then south into northern Argentina and Peru (Wilson and Reeder, 1993).

Bats

Conflict of interest statement

All the authors declare no conflicts of interest related to this article.

Acknowledgments

This study was supported by the AMIDEX project (No. ANR-11-IDEX-0001-02) funded by the “Investissements d’Avenir,” a French Government program managed by the French National Research Agency (ANR) and Foundation Méditerranée Infection (www.mediterranee-infection.com). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. This work was also supported by the medical service of the French armed forces. We thank Annick Abeille

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