Interactions between Asaia, Plasmodium and Anopheles: new insights into mosquito symbiosis and implications in Malaria Symbiotic Control

Capone, Aida; Ricci, Irene; Damiani, Claudia; Mosca, Monica; Rossi, Paolo; Scuppa, Patrizia; Crotti, Elena; Epis, Sara; Angeletti, Mauro; Valzano, Matteo; Sacchi, Luciano; Bandi, Claudio; Daffonchio, Daniele; Mandrioli, Mauro; Favia, Guido

doi:10.1186/1756-3305-6-182

Cited by 79 publications

(64 citation statements)

References 33 publications

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“…Furthermore, environmental pollution and resistance phenomena clearly show the limits of the chemical approach for pest control and the need to delineate new strategies that optimize the use of available molecules, with the aim of reducing their impact on the environment [31, 45–48]. …”

Section: Discussionmentioning

confidence: 99%

ABC transporters are involved in defense against permethrin insecticide in the malaria vector Anopheles stephensi

et al. 2014

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BackgroundProteins from the ABC family (ATP-binding cassette) represent the largest known group of efflux pumps, responsible for transporting specific molecules across lipid membranes in both prokaryotic and eukaryotic organisms. In arthropods they have been shown to play a role in insecticide defense/resistance. The presence of ABC transporters and their possible association with insecticide transport have not yet been investigated in the mosquito Anopheles stephensi, the major vector of human malaria in the Middle East and South Asian regions. Here we investigated the presence and role of ABCs in transport of permethrin insecticide in a susceptible strain of this mosquito species.MethodsTo identify ABC transporter genes we obtained a transcriptome from untreated larvae of An. stephensi and then compared it with the annotated transcriptome of Anopheles gambiae. To analyse the association between ABC transporters and permethrin we conducted bioassays with permethrin alone and in combination with an ABC inhibitor, and then we investigated expression profiles of the identified genes in larvae exposed to permethrin.ResultsBioassays showed an increased mortality of mosquitoes when permethrin was used in combination with the ABC-transporter inhibitor. Genes for ABC transporters were detected in the transcriptome, and five were selected (AnstABCB2, AnstABCB3, AnstABCB4, AnstABCmember6 and AnstABCG4). An increased expression in one of them (AnstABCG4) was observed in larvae exposed to the LD50 dose of permethrin. Contrary to what was found in other insect species, no up-regulation was observed in the AnstABCB genes.ConclusionsOur results show for the first time the involvement of ABC transporters in larval defense against permethrin in An. stephensi and, more in general, confirm the role of ABC transporters in insecticide defense. The differences observed with previous studies highlight the need of further research as, despite the growing number of studies on ABC transporters in insects, the heterogeneity of the results available at present does not allow us to infer general trends in ABC transporter-insecticide interactions.Electronic supplementary materialThe online version of this article (doi:10.1186/1756-3305-7-349) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

ABC transporters are involved in defense against permethrin insecticide in the malaria vector Anopheles stephensi

et al. 2014

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“…Asaia species have previously not been identified in Culicoides. Asaia has been detected in Anopheles mosquitoes, colonizing the salivary glands and midgut of the insect (46). Unlike Wolbachia and Cardinium, Asaia species can be cultured on medium and easily colonize insects.…”

Section: Discussionmentioning

confidence: 99%

“…Unlike Wolbachia and Cardinium, Asaia species can be cultured on medium and easily colonize insects. Hence, these bacteria have been suggested as potential paratransgenesis control agents for insect vectors (46,47).…”

Section: Discussionmentioning

confidence: 99%

Detection of Low-Level Cardinium and Wolbachia Infections in Culicoides

Mee

Weeks

Walker

et al. 2015

Appl Environ Microbiol

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bBacterial endosymbionts have been identified as potentially useful biological control agents for a range of invertebrate vectors of disease. Previous studies of Culicoides (Diptera: Ceratopogonidae) species using conventional PCR assays have provided evidence of Wolbachia (1/33) and Cardinium (8/33) infections. Here, we screened 20 species of Culicoides for Wolbachia and Cardinium, utilizing a combination of conventional PCR and more sensitive quantitative PCR (qPCR) assays. Low levels of Cardinium DNA were detected in females of all but one of the Culicoides species screened, and low levels of Wolbachia were detected in females of 9 of the 20 Culicoides species. Sequence analysis based on partial 16S rRNA gene and gyrB sequences identified "Candidatus Cardinium hertigii" from group C, which has previously been identified in Culicoides from Japan, Israel, and the United Kingdom. Wolbachia strains detected in this study showed 98 to 99% sequence identity to Wolbachia previously detected from Culicoides based on the 16S rRNA gene, whereas a strain with a novel wsp sequence was identified in Culicoides narrabeenensis. Cardinium isolates grouped to geographical regions independent of the host Culicoides species, suggesting possible geographical barriers to Cardinium movement. Screening also identified Asaia bacteria in Culicoides. These findings point to a diversity of low-level endosymbiont infections in Culicoides, providing candidates for further characterization and highlighting the widespread occurrence of these endosymbionts in this insect group.

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“…Recent evidence is mounting that the transmission of vector‐borne pathogens can be inhibited by other vector‐associated microbes (Sinkins, 2013). In the past decade, studies have shown that certain microbes associated with insect vectors could be used to mediate the transmission of diseases including those transmitted by mosquitoes (Capone et al., 2013; Cirimotich et al., 2011; Dong, Manfredini, & Dimopoulos, 2009; Mourya, Pidiyar, Patole, Gokhale, & Shouche, 2002; Ramirez et al., 2014; Tchioffo et al., 2013; Xi, Ramirez, & Dimopoulos, 2008), tsetse flies (Pais, Lohs, Wu, Wang, & Aksoy, 2008; Wang, Wu, Yang, & Aksoy, 2009; Weiss, Wang, Maltz, Wu, & Aksoy, 2013), sand flies (Sant'Anna et al., 2014), and ticks (Gall et al., 2016; Narasimhan et al., 2014). The most striking example is the inhibition by bacterium Wolbachia pipientis of virus and parasite infection in mosquito vectors (Bian, Xu, Lu, Xie, & Xi, 2010; Blagrove, Arias‐Goeta, Di Genua, Failloux, & Sinkins, 2013; Frentiu et al., 2014; van den Hurk et al., 2012; Hussain et al., 2012; Moreira et al., 2009).…”

Section: Introductionmentioning

confidence: 99%

Mosquito vector‐associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod‐borne diseases

Thongsripong

Chandler

Green

et al. 2017

Ecology and Evolution

109

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Vector‐borne diseases are a major health burden, yet factors affecting their spread are only partially understood. For example, microbial symbionts can impact mosquito reproduction, survival, and vectorial capacity, and hence affect disease transmission. Nonetheless, current knowledge of mosquito‐associated microbial communities is limited. To characterize the bacterial and eukaryotic microbial communities of multiple vector species collected from different habitat types in disease endemic areas, we employed next‐generation 454 pyrosequencing of 16S and 18S rRNA amplicon libraries, also known as metabarcoding. We investigated pooled whole adult mosquitoes of three medically important vectors, Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus, collected from different habitats across central Thailand where we previously characterized mosquito diversity. Our results indicate that diversity within the mosquito microbiota is low, with the majority of microbes assigned to one or a few taxa. Two of the most common eukaryotic and bacterial genera recovered (Ascogregarina and Wolbachia, respectively) are known mosquito endosymbionts with potentially parasitic and long evolutionary relationships with their hosts. Patterns of microbial composition and diversity appeared to differ by both vector species and habitat for a given species, although high variability between samples suggests a strong stochastic element to microbiota assembly. In general, our findings suggest that multiple factors, such as habitat condition and mosquito species identity, may influence overall microbial community composition, and thus provide a basis for further investigations into the interactions between vectors, their microbial communities, and human‐impacted landscapes that may ultimately affect vector‐borne disease risk.

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Interactions between Asaia, Plasmodium and Anopheles: new insights into mosquito symbiosis and implications in Malaria Symbiotic Control

Cited by 79 publications

References 33 publications

ABC transporters are involved in defense against permethrin insecticide in the malaria vector Anopheles stephensi

ABC transporters are involved in defense against permethrin insecticide in the malaria vector Anopheles stephensi

Detection of Low-Level Cardinium and Wolbachia Infections in Culicoides

Mosquito vector‐associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod‐borne diseases

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