Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections

Abstract

BackgroundThe native gut microbiota of Anopheles mosquitoes is known to play a key role in the physiological function of its host. Interestingly, this microbiota can also influence the development of Plasmodium in its host mosquitoes. In recent years, much interest has been shown in the employment of gut symbionts derived from vectors in the control of vector-borne disease transmission. In this study, the midgut microbial diversity has been characterized among laboratory-reared adult Anopheles stephensi mosquitoes, from the colony created by rearing progeny of wild-caught mosquitoes (obtained from three different locations in southern India) for multiple generations, using 16S ribosomal RNA (rRNA) gene sequencing approach. Further, the influence of native midgut microbiota of mosquitoes on the development of rodent malaria parasite Plasmodium berghei in its host has been studied.MethodsThe microbial diversity associated with the midgut of An. stephensi mosquitoes was studied by sequencing V3 region of 16S ribosomal RNA (rRNA) gene. The influence of native midgut microbiota of An. stephensi mosquitoes on the susceptibility of the mosquitoes to rodent malaria parasite P. berghei was studied by comparing the intensity and prevalence of P. berghei infection among the antibiotic treated and untreated cohorts of mosquitoes.ResultsThe analysis of bacterial diversity from the midguts of An. stephensi showed Proteobacteria as the most dominant population among the three laboratory-reared strains of An. stephensi studied. Major genera identified among these mosquito strains were Acinetobacter, Pseudomonas, Prevotella, Corynebacterium, Veillonella, and Bacillus. The mosquito infectivity studies carried out to determine the implication of total midgut microbiota on P. berghei infection showed that mosquitoes whose native microbiota cleared with antibiotics had increased susceptibility to P. berghei infection compared to the antibiotic untreated mosquitoes with its natural native microbiota.ConclusionsThe use of microbial symbiont to reduce the competence of vectors involved in disease transmission has gained much importance in recent years as an emerging alternative approach towards disease control. In this context, the present study was aimed to identify the midgut microbiota composition of An. stephensi, and its effect on the development of P. berghei. Interestingly, the analysis of midgut microbiota from An. stephensi revealed the presence of genus Veillonella in Anopheles species for the first time. Importantly, the study also revealed the negative influence of total midgut microbiota on the development of P. berghei in three laboratory strains of An. stephensi, emphasizing the importance of understanding the gut microbiota in malaria vectors, and its relationship with parasite development in designing strategies to control malaria transmission.Electronic supplementary materialThe online version of this article (10.1186/s12936-018-2535-7) contains supplementary material, which is available to authorized users.

The Aedes albopictus (Diptera: Culicidae) microbiome varies spatially and with Ascogregarine infection

“…The infection of A. taiwanensis occurs in the early aquatic life stages of mosquitoes [20,21] and thus proceeds through several tissues in the mosquito that are also important for the persistence and transstadial transmission of environmentally acquired bacterial symbionts, and may explain the compositional changes in the environmentally acquired bacterial microbiome [20,21,56]. For instance, the initial site of A. taiwanensis infection is the mosquito midgut, which harbors a diverse assemblage of symbionts and is a major site of primary colonization of environmentally acquired bacteria in the mosquito [8,13]. In addition, the Malpighian tubules, which harbor A. taiwanensis, are conserved during metamorphosis at the pupal stage and have been implicated in the transstadial transmission of symbionts acquired during the larval stage to the adult stage, where disease transmission occurs [57].…”

“…mosquitoes to arboviruses and Plasmodium sp., respectively [10][11][12]. This change in vector competence might be associated with competition between microbial symbionts for resources, the release of anti-pathogen peptides that directly limit pathogen growth and extend the incubation period, or through the regulation of specific components of the insect immune system [8,13].…”

Comparison of infectivity of Plasmodium vivax to wild-caught and laboratory-adapted (colonized) Anopheles arabiensis mosquitoes in Ethiopia

“…These factors range from mosquito genetics [27,28] and immune system [29] to parasite polymorphisms that allow evasion of the mosquito immune system [30]. Environmental factors such as midgut microbiota [31,32], mosquito larval diet [33,34], and temperature to support sporogony [35] are also implicated. These findings emphasize that infectivity studies from colony mosquitoes might not represent the infectivity in natural settings and therefore, assessment of the relative permissiveness of colony and wild mosquitoes could assist in the interpretation of mosquito-feeding assays to the local context.…”

Second generation effects of larval metal pollutant exposure on reproduction, longevity and insecticide tolerance in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)

“…This includes range expansion into polluted environments and increased insecticide resistance levels [11,24]. There is also evidence that pollutants alter the gut microbiome [45,46] which could affect vector competence [47][48][49]. Added to these findings are the data presented here showing that single exposures to heavy metal pollution can have transgenerational effects on insecticide resistance, although these effects differed between the insecticide-susceptible SENN and insecticide-resistant SENN-DDT strains.…”