Metabolic interactions between disease-transmitting vectors and their microbiota

Song, Xinmao; Zhong, Zhengwei; Gao, Li; Weiss, Brian L.; Wang, Jingwen

doi:10.1016/j.pt.2022.05.002

Cited by 28 publications

(18 citation statements)

References 100 publications

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“…The functional aspects of the bacterial microbiota of blood-feeding arthropods, integrating their metabolic products with their physiology, has started to emerge, as reviewed by ( Song et al., 2022 ). The metabolic interaction between bacteria and ticks, with a distinct impact on development and/or physiology, seems to be very species-specific ( Duron et al., 2018 ; Zhong et al., 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Ixodes ricinus ticks have a functional association with Midichloria mitochondrii

Guizzo

Hatalová

Frantová

et al. 2023

Front. Cell. Infect. Microbiol.

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In addition to being vectors of pathogenic bacteria, ticks also harbor intracellular bacteria that associate with ticks over generations, aka symbionts. The biological significance of such bacterial symbiosis has been described in several tick species but its function in Ixodes ricinus is not understood. We have previously shown that I. ricinus ticks are primarily inhabited by a single species of symbiont, Midichloria mitochondrii, an intracellular bacterium that resides and reproduces mainly in the mitochondria of ovaries of fully engorged I. ricinus females. To study the functional integration of M. mitochondrii into the biology of I. ricinus, an M. mitochondrii-depleted model of I. ricinus ticks was sought. Various techniques have been described in the literature to achieve dysbiosed or apo-symbiotic ticks with various degrees of success. To address the lack of a standardized experimental procedure for the production of apo-symbiotic ticks, we present here an approach utilizing the ex vivo membrane blood feeding system. In order to deplete M. mitochondrii from ovaries, we supplemented dietary blood with tetracycline. We noted, however, that the use of tetracycline caused immediate toxicity in ticks, caused by impairment of mitochondrial proteosynthesis. To overcome the tetracycline-mediated off-target effect, we established a protocol that leads to the production of an apo-symbiotic strain of I. ricinus, which can be sustained in subsequent generations. In two generations following tetracycline administration and tetracycline-mediated symbiont reduction, M. mitochondrii was gradually eliminated from the lineage. Larvae hatched from eggs laid by such M. mitochondrii-free females repeatedly performed poorly during blood-feeding, while the nymphs and adults performed similarly to controls. These data indicate that M. mitochondrii represents an integral component of tick ovarian tissue, and when absent, results in the formation of substandard larvae with reduced capacity to blood-feed.

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Section: Discussionmentioning

confidence: 99%

Ixodes ricinus ticks have a functional association with Midichloria mitochondrii

Guizzo

Hatalová

Frantová

et al. 2023

Front. Cell. Infect. Microbiol.

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“…Members of genus Asaia are commonly present in different mosquito species [ 69 , 70 ]. Bacteria in this genus are known to interact with resident microbiota [ 71 , 72 ] and to influence vector metabolism [ 73 ]. In particular, Asaia was found to modulate midgut pH through glucose metabolism in the Anopheles vector, which in turn promotes Plasmodium microgametogenesis (i.e.…”

Section: Discussionmentioning

confidence: 99%

Immune-related transcripts, microbiota and vector competence differ in dengue-2 virus-infected geographically distinct Aedes aegypti populations

et al. 2023

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Background Vector competence in Aedes aegypti is influenced by various factors. Crucial new control methods can be developed by recognizing which factors affect virus and mosquito interactions. Methods In the present study we used three geographically distinct Ae. aegypti populations and compared their susceptibility to infection by dengue virus serotype 2 (DENV-2). To identify any differences among the three mosquito populations, we evaluated expression levels of immune-related genes and assessed the presence of microbiota that might contribute to the uniqueness in their vector competence. Results Based on the results from the DENV-2 competence study, we categorized the three geographically distinct Ae. aegypti populations into a refractory population (Vilas do Atlântico), a susceptible population (Vero) and a susceptible but low transmission population (California). The immune-related transcripts were highly expressed in the California population but not in the refractory population. However, the Rel-1 gene was upregulated in the Vilas do Atlântico population following ingestion of a non-infectious blood meal, suggesting the gene’s involvement in non-viral responses, such as response to microbiota. Screening of the bacteria, fungi and flaviviruses revealed differences between populations, and any of these could be one of the factors that interfere with the vector competence. Conclusions The results reveal potential factors that might impact the virus and mosquito interaction, as well as influence the Ae. aegypti refractory phenotype. Graphical Abstract

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“…Asaia are commonly present in different mosquito species [69,70]. Bacteria in this genus are known to interact with resident microbiota [71,72] and to in uence vector metabolism [73]. Particularly, Asaia was found to modulate midgut pH through glucose metabolism in the Anopheles vector, which in turn promotes Plasmodium microgametogenesis (i.e., development of male gametes), a critical step in the malaria-parasite life cycle that when increased enhances infection of the mosquito midgut [74].…”

Section: Discussionmentioning

confidence: 99%

Immune-related transcripts, microbiota and vector competence differ in dengue-infected geographically distinct Aedes aegypti populations

Chen

Bozic

Mathias

et al. 2023

Preprint

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Background Vector competence in Aedes aegypti is influenced by various factors and, by recognizing what affects virus and mosquito interactions, crucial new control methods can be developed. Methods Here we used three geographically distinct Ae. aegypti populations and compared their susceptibility to infection by dengue virus (DENV). To identify the population differences, we screened immune-related genes and microbiota which might contribute to the uniqueness in competency. Results Based on the results from the DENV competence study, we assigned a refractory population (Vilas do Atlântico), a susceptible population (Vero), and a susceptible but low transmission population (California). The immune-related transcripts were highly expressed in the California population but not in the refractory population. However, the Rel-1 gene upregulated after blood-feeding in the Vilas do Atlântico population suggesting involvement in non-viral responses, such as response to microbiota. The bacteria, fungi, and flaviviruses screening showed differences between populations and could be one of the factors that interfere with the vector competence. Conclusions All in all, we revealed the potential factors that might impact the virus and mosquito interaction, moreover, influencing the Aedes aegypti refractory phenotype.

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Metabolic interactions between disease-transmitting vectors and their microbiota

Cited by 28 publications

References 100 publications

Ixodes ricinus ticks have a functional association with Midichloria mitochondrii

Ixodes ricinus ticks have a functional association with Midichloria mitochondrii

Immune-related transcripts, microbiota and vector competence differ in dengue-2 virus-infected geographically distinct Aedes aegypti populations

Immune-related transcripts, microbiota and vector competence differ in dengue-infected geographically distinct Aedes aegypti populations

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