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Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases

View Article: PubMed Central - PubMed

ABSTRACT

Ticks and the pathogens they transmit constitute a growing burden for human and animal health worldwide. Vector competence is a component of vectorial capacity and depends on genetic determinants affecting the ability of a vector to transmit a pathogen. These determinants affect traits such as tick-host-pathogen and susceptibility to pathogen infection. Therefore, the elucidation of the mechanisms involved in tick-pathogen interactions that affect vector competence is essential for the identification of molecular drivers for tick-borne diseases. In this review, we provide a comprehensive overview of tick-pathogen molecular interactions for bacteria, viruses, and protozoa affecting human and animal health. Additionally, the impact of tick microbiome on these interactions was considered. Results show that different pathogens evolved similar strategies such as manipulation of the immune response to infect vectors and facilitate multiplication and transmission. Furthermore, some of these strategies may be used by pathogens to infect both tick and mammalian hosts. Identification of interactions that promote tick survival, spread, and pathogen transmission provides the opportunity to disrupt these interactions and lead to a reduction in tick burden and the prevalence of tick-borne diseases. Targeting some of the similar mechanisms used by the pathogens for infection and transmission by ticks may assist in development of preventative strategies against multiple tick-borne diseases.

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Possible impact of tick microbiome on pathogen transmission. Tick microbiome may affect pathogen transmission either directly via nutrient competition or induced/reduced immunity, or indirectly by affecting tick populations (viability, reproduction) or fitness (affecting host-seeking success). MG, midgut; SG, salivary gland; OV, ovaries.
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Figure 3: Possible impact of tick microbiome on pathogen transmission. Tick microbiome may affect pathogen transmission either directly via nutrient competition or induced/reduced immunity, or indirectly by affecting tick populations (viability, reproduction) or fitness (affecting host-seeking success). MG, midgut; SG, salivary gland; OV, ovaries.

Mentions: Symbionts may confer crucial and diverse benefits to their hosts, playing nutritional roles, or affecting fitness, development, reproduction, defense against environmental stress, and immunity (Ahantarig et al., 2013). Coxiella-like endosymbionts are believed to be the most common vertically transmitted agents in hard ticks (Bernasconi et al., 2002; Lee et al., 2004; Clay et al., 2008; Bonnet et al., 2013; Cooper et al., 2013). In Amblyomma americanum, the removal of Coxiella symbionts following antibiotic treatment reduced tick offspring production and increased time to oviposition (Zhong et al., 2007). In I. ricinus (Lo et al., 2006; Sassera et al., 2006; Montagna et al., 2013), Candidatus Midichloria mitochondrii is an intra-mitochondrial bacterium that has also been detected in other tick genera (Harrus et al., 2011; Williams-Newkirk et al., 2012). It has been ascribed a possible helper role in tick molting processes (Zchori-Fein and Bourtzis, 2011, Figure 3). Rickettsia-like symbionts have also been reported to infect hard ticks from several genera (Baldridge et al., 2004; Clay et al., 2008; Liu et al., 2013). One study reported that Rickettsia-infected Dermacentor variabilis have slightly greater motility than uninfected ticks, indirectly influencing disease risk (Kagemann and Clay, 2013). Francisella-like symbionts have been reported in several hard tick genera (Venzal et al., 2008; Ivanov et al., 2011; Michelet et al., 2013), but their effect on tick fitness and biology remains unknown. Being able to manipulate host reproduction and then to affect vector populations, Wolbachia spp. have also been identified in several hard tick genera (Engelstadter and Hurst, 2007; Andreotti et al., 2011; Reis et al., 2011; Zhang X. et al., 2011). Their role in pathogen transmission requires further attention, as reports suggest that this bacterium can protect some arthropods against microbial infections (Martinez et al., 2014). In I. ricinus, Wolbachia pipientis is known to be associated with the hymenoptera tick endoparasitoid Ixodiphagus hookeri (Plantard et al., 2012; Bohacsova et al., 2016), and Arsenophonus spp. symbionts (Dergousoff and Chilton, 2010). The latter, detected in several tick species (Clay et al., 2008; Dergousoff and Chilton, 2010; Reis et al., 2011), are responsible for sex-ratio distortion in arthropods, and some studies suggest that they can affect host-seeking success by decreasing tick motility in A. americanum and D. variabilis (Kagemann and Clay, 2013). Lastly, some Spiroplasma spp. detected in Ixodes spp. such as Spiroplasma ixodetis (Tully et al., 1995) may cause sex-ratio distortion in some insect species via male killing (Tabata et al., 2011).


Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases
Possible impact of tick microbiome on pathogen transmission. Tick microbiome may affect pathogen transmission either directly via nutrient competition or induced/reduced immunity, or indirectly by affecting tick populations (viability, reproduction) or fitness (affecting host-seeking success). MG, midgut; SG, salivary gland; OV, ovaries.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5383669&req=5

Figure 3: Possible impact of tick microbiome on pathogen transmission. Tick microbiome may affect pathogen transmission either directly via nutrient competition or induced/reduced immunity, or indirectly by affecting tick populations (viability, reproduction) or fitness (affecting host-seeking success). MG, midgut; SG, salivary gland; OV, ovaries.
Mentions: Symbionts may confer crucial and diverse benefits to their hosts, playing nutritional roles, or affecting fitness, development, reproduction, defense against environmental stress, and immunity (Ahantarig et al., 2013). Coxiella-like endosymbionts are believed to be the most common vertically transmitted agents in hard ticks (Bernasconi et al., 2002; Lee et al., 2004; Clay et al., 2008; Bonnet et al., 2013; Cooper et al., 2013). In Amblyomma americanum, the removal of Coxiella symbionts following antibiotic treatment reduced tick offspring production and increased time to oviposition (Zhong et al., 2007). In I. ricinus (Lo et al., 2006; Sassera et al., 2006; Montagna et al., 2013), Candidatus Midichloria mitochondrii is an intra-mitochondrial bacterium that has also been detected in other tick genera (Harrus et al., 2011; Williams-Newkirk et al., 2012). It has been ascribed a possible helper role in tick molting processes (Zchori-Fein and Bourtzis, 2011, Figure 3). Rickettsia-like symbionts have also been reported to infect hard ticks from several genera (Baldridge et al., 2004; Clay et al., 2008; Liu et al., 2013). One study reported that Rickettsia-infected Dermacentor variabilis have slightly greater motility than uninfected ticks, indirectly influencing disease risk (Kagemann and Clay, 2013). Francisella-like symbionts have been reported in several hard tick genera (Venzal et al., 2008; Ivanov et al., 2011; Michelet et al., 2013), but their effect on tick fitness and biology remains unknown. Being able to manipulate host reproduction and then to affect vector populations, Wolbachia spp. have also been identified in several hard tick genera (Engelstadter and Hurst, 2007; Andreotti et al., 2011; Reis et al., 2011; Zhang X. et al., 2011). Their role in pathogen transmission requires further attention, as reports suggest that this bacterium can protect some arthropods against microbial infections (Martinez et al., 2014). In I. ricinus, Wolbachia pipientis is known to be associated with the hymenoptera tick endoparasitoid Ixodiphagus hookeri (Plantard et al., 2012; Bohacsova et al., 2016), and Arsenophonus spp. symbionts (Dergousoff and Chilton, 2010). The latter, detected in several tick species (Clay et al., 2008; Dergousoff and Chilton, 2010; Reis et al., 2011), are responsible for sex-ratio distortion in arthropods, and some studies suggest that they can affect host-seeking success by decreasing tick motility in A. americanum and D. variabilis (Kagemann and Clay, 2013). Lastly, some Spiroplasma spp. detected in Ixodes spp. such as Spiroplasma ixodetis (Tully et al., 1995) may cause sex-ratio distortion in some insect species via male killing (Tabata et al., 2011).

View Article: PubMed Central - PubMed

ABSTRACT

Ticks and the pathogens they transmit constitute a growing burden for human and animal health worldwide. Vector competence is a component of vectorial capacity and depends on genetic determinants affecting the ability of a vector to transmit a pathogen. These determinants affect traits such as tick-host-pathogen and susceptibility to pathogen infection. Therefore, the elucidation of the mechanisms involved in tick-pathogen interactions that affect vector competence is essential for the identification of molecular drivers for tick-borne diseases. In this review, we provide a comprehensive overview of tick-pathogen molecular interactions for bacteria, viruses, and protozoa affecting human and animal health. Additionally, the impact of tick microbiome on these interactions was considered. Results show that different pathogens evolved similar strategies such as manipulation of the immune response to infect vectors and facilitate multiplication and transmission. Furthermore, some of these strategies may be used by pathogens to infect both tick and mammalian hosts. Identification of interactions that promote tick survival, spread, and pathogen transmission provides the opportunity to disrupt these interactions and lead to a reduction in tick burden and the prevalence of tick-borne diseases. Targeting some of the similar mechanisms used by the pathogens for infection and transmission by ticks may assist in development of preventative strategies against multiple tick-borne diseases.

No MeSH data available.


Related in: MedlinePlus