Detection of New Francisella-Like Tick Endosymbionts in Hyalomma spp. and Rhipicephalus spp. (Acari: Ixodidae) from Bulgaria

Ivanov, Ivanov N.; Mitkova, Nadia; Reye, Anna L.; Hübschen, Judith M.; Vatcheva-Dobrevska, Rossitza; Dobreva, Elina; Kantardjiev, Todor; Muller, Claude P.

doi:10.1128/aem.02934-10

Cited by 61 publications

(53 citation statements)

References 19 publications

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“…Second, the 16S rRNA-based phylogenetic analysis demonstrated that the FLE from Hyalomma ticks are clustered together as a monophyletic group separated from pathogenic Francisella spp., in agreement with other FLE phylogeny analyses (9,29,33,34), and the phylogenetic congruence between FLE and their Hyalomma hosts is significant. The sequences of FLE from H. marginatum and H. rufipes were identical, as was shown previously (10,29).…”

Section: Discussionsupporting

confidence: 73%

“…Our results support the assumption that FLE are obligatory symbionts of their Hyalomma hosts. First, FLE was found to be highly prevalent across all Hyalomma species screened, including H. marginatum, whereas other studies reported lower FLE prevalence (9,29). This difference, however, might be explained by method sensitivity, or the possibility that FLE have a different importance in Hyalomma ticks from different areas.…”

Section: Discussioncontrasting

confidence: 42%

“…carry Francisella-like endosymbionts (FLE) (8)(9)(10) that may be obligatory primary symbionts supporting the restricted blood diet, as with other ticks and hematophagous insects (11). Several endosymbiotic bacteria in arthropod vectors were shown to interact with pathogens and affect their host's susceptibility to infection, including in tick hosts (12)(13)(14).…”

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Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

Azagi

Klement

Perlman

et al. 2017

Appl Environ Microbiol

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Hyalomma ticks (Acari: Ixodidae) are hosts for Francisella-like endosymbionts (FLE) and may serve as vectors of zoonotic disease agents. This study aimed to provide an initial characterization of the interaction between Hyalomma and FLE and to determine the prevalence of pathogenic Rickettsia in these ticks. Hyalomma marginatum, Hyalomma rufipes, Hyalomma dromedarii, Hyalomma aegyptium, and Hyalomma excavatum ticks, identified morphologically and molecularly, were collected from different hosts and locations representing the distribution of the genus Hyalomma in Israel, as well as from migratory birds. A high prevalence of FLE was found in all Hyalomma species (90.6%), as well as efficient maternal transmission of FLE (91.8%), and the localization of FLE in Malpighian tubules, ovaries, and salivary glands in H. marginatum. Furthermore, we demonstrated strong cophylogeny between FLE and their host species. Contrary to FLE, the prevalence of Rickettsia ranged from 2.4% to 81.3% and was significantly different between Hyalomma species, with a higher prevalence in ticks collected from migratory birds. Using ompA gene sequences, most of the Rickettsia spp. were similar to Rickettsia aeschlimannii, while a few were similar to Rickettsia africae of the spotted fever group (SFG). Given their zoonotic importance, 249 ticks were tested for Crimean Congo hemorrhagic fever virus infection, and all were negative. The results imply that Hyalomma and FLE have obligatory symbiotic interactions, indicating a potential SFG Rickettsia zoonosis risk. A further understanding of the possible influence of FLE on Hyalomma development, as well as on its infection with Rickettsia pathogens, may lead to novel ways to control tick-borne zoonoses.IMPORTANCE This study shows that Francisella-like endosymbionts were ubiquitous in Hyalomma, were maternally transmitted, and cospeciated with their hosts. These findings imply that the interaction between FLE and Hyalomma is of an obligatory nature. It provides an example of an integrative taxonomy approach to simply differentiate among species infesting the same host and to identify nymphal and larval stages to be used in further studies. In addition, it shows the potential of imported Hyalomma ticks to serve as a vector for spotted fever group rickettsiae. The information gathered in this study can be further implemented in the development of symbiont-based disease control strategies for the benefit of human health.

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Section: Discussionsupporting

confidence: 73%

Section: Discussioncontrasting

confidence: 42%

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Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

Azagi

Klement

Perlman

et al. 2017

Appl Environ Microbiol

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“…Recent investigation of 295 dogs for ticks revealed an infestations rate of 23.7 % for ticks, with Rhipicephalus sanguineus and Ixodes ricinus found in 19.7 % and 6.4 % of the dogs respectively, while obviously no Dermacentor reticulatus ticks were identified (Kirkova et al 2013). These data were in part confirmed by another study investigating ticks (n = 472) collected from humans (n = 32), animals (n = 264) and environment (n = 176) in nine major districts in Bulgaria (Ivanov et al 2011). Latter study revealed R. sanguineus in 31.4 % (148/472) and I. ricinus in 25.4 % (120/472) of the cases, but also D. reticulatus was found, even though at a lower rate (3.6 %; 17/472).…”

Section: Introductionsupporting

confidence: 69%

Current Surveys of the Seroprevalence of Borrelia burgdorferi, Ehrlichia canis, Anaplasma phagocytophilum, Leishmania infantum, Babesia canis, Angiostrongylus vasorum and Dirofilaria immitis in Dogs in Bulgaria

et al. 2015

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Canine vector-borne diseases (CVBDs) have increasingly become a focus of interest in recent years. Some of the CVBDs are zoonotic and may therefore also represent a risk for the human population. Different factors are in discussion to explain the expansion of vectors and pathogens into formerly unaffected areas. Knowledge of the prevalence and distribution of CVBDs in Bulgaria is scant overall and most data rely on single case descriptions. The aim of the present study was to determine the seroprevalence of important CVBDs in 167 dogs from central-southern Bulgaria (Stara Zagora), with special emphasis on hitherto uninvestigated babesiosis and angiostrongylosis, on poorly investigated Lyme borreliosis and canine granulocytic anaplasmosis, and on the potentially zoonotic dirofilariosis and leishmaniosis. Relatively high prevalence rates were documented for anti-Babesia canis antibodies, Dirofilaria immitis antigen (16.2 %; 27/167 each), anti-Ehrlichia canis (21 %; 35/167) and anti-Anaplasma phagocytophilum antibodies (30.5 -46.1 %; 51 -77/167), while Borrelia burgdorferi seroprevalence was low (2.4 %; 4/167). All samples were negative for Leishmania infantum antibodies and Angiostrongylus vasorum antigen and antibodies. In total, 64.7 % (108/167) of the samples indicated infection or exposure to at least one agent and a high proportion of dual infections (39.8 %; 43/108) was demonstrated. Multiple infections with up to four different organisms were also detected. Our data underline the importance of CVBDs and especially of co-infections which could influence the clinical outcome in dogs. (2015) 114 :S11 -S1 DOI 10.1007/s00436-015-4518-8 EcToPaR aSITES AbstractCanine vector-borne diseases (CVBDs) have increasingly become a focus of interest in recent years. Some of the CVBDs are zoonotic and may therefore also represent a risk for the human population. Different factors are in discussion to explain the expansion of vectors and pathogens into formerly unaffected areas. Knowledge of the prevalence and distribution of CVBDs in Bulgaria is scant overall and most data rely on single case descriptions.

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“…To date, a wide range of symbionts, such as Coxiella-like (13), Francisella-like (14), Wolbachia-like (15), Rickettsia-like (16), Arsenophonus-like (17), "Candidatus Midichloria mitochondrii" (18), and Rickettsia peacockii (19) symbionts, have been detected in several tick species. However, little attention has been given to coinfection with multiple symbionts of ticks.…”

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Coinfection of Dermacentor silvarum Olenev (Acari: Ixodidae) by Coxiella-Like, Arsenophonus-Like, and Rickettsia-Like Symbionts

Liu

et al. 2013

Appl Environ Microbiol

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Detection of New Francisella-Like Tick Endosymbionts in Hyalomma spp. and Rhipicephalus spp. (Acari: Ixodidae) from Bulgaria

Cited by 61 publications

References 19 publications

Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

Current Surveys of the Seroprevalence of Borrelia burgdorferi, Ehrlichia canis, Anaplasma phagocytophilum, Leishmania infantum, Babesia canis, Angiostrongylus vasorum and Dirofilaria immitis in Dogs in Bulgaria

Coinfection of Dermacentor silvarum Olenev (Acari: Ixodidae) by Coxiella-Like, Arsenophonus-Like, and Rickettsia-Like Symbionts

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