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Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections

BACKGROUND: The 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...

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Autores principales: Kalappa, Devaiah Monnanda, Subramani, Pradeep Annamalai, Basavanna, Sowmya Kanchanahalli, Ghosh, Susanta Kumar, Sundaramurthy, Varadharajan, Uragayala, Sreehari, Tiwari, Satyanarayan, Anvikar, Anupkumar R., Valecha, Neena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6203276/
https://www.ncbi.nlm.nih.gov/pubmed/30359252
http://dx.doi.org/10.1186/s12936-018-2535-7
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author Kalappa, Devaiah Monnanda
Subramani, Pradeep Annamalai
Basavanna, Sowmya Kanchanahalli
Ghosh, Susanta Kumar
Sundaramurthy, Varadharajan
Uragayala, Sreehari
Tiwari, Satyanarayan
Anvikar, Anupkumar R.
Valecha, Neena
author_facet Kalappa, Devaiah Monnanda
Subramani, Pradeep Annamalai
Basavanna, Sowmya Kanchanahalli
Ghosh, Susanta Kumar
Sundaramurthy, Varadharajan
Uragayala, Sreehari
Tiwari, Satyanarayan
Anvikar, Anupkumar R.
Valecha, Neena
author_sort Kalappa, Devaiah Monnanda
collection PubMed
description BACKGROUND: The 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. METHODS: The 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. RESULTS: The 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. CONCLUSIONS: The 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 MATERIAL: The online version of this article (10.1186/s12936-018-2535-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-62032762018-11-01 Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections Kalappa, Devaiah Monnanda Subramani, Pradeep Annamalai Basavanna, Sowmya Kanchanahalli Ghosh, Susanta Kumar Sundaramurthy, Varadharajan Uragayala, Sreehari Tiwari, Satyanarayan Anvikar, Anupkumar R. Valecha, Neena Malar J Research BACKGROUND: The 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. METHODS: The 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. RESULTS: The 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. CONCLUSIONS: The 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 MATERIAL: The online version of this article (10.1186/s12936-018-2535-7) contains supplementary material, which is available to authorized users. BioMed Central 2018-10-25 /pmc/articles/PMC6203276/ /pubmed/30359252 http://dx.doi.org/10.1186/s12936-018-2535-7 Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Kalappa, Devaiah Monnanda
Subramani, Pradeep Annamalai
Basavanna, Sowmya Kanchanahalli
Ghosh, Susanta Kumar
Sundaramurthy, Varadharajan
Uragayala, Sreehari
Tiwari, Satyanarayan
Anvikar, Anupkumar R.
Valecha, Neena
Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections
title Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections
title_full Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections
title_fullStr Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections
title_full_unstemmed Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections
title_short Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections
title_sort influence of midgut microbiota in anopheles stephensi on plasmodium berghei infections
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6203276/
https://www.ncbi.nlm.nih.gov/pubmed/30359252
http://dx.doi.org/10.1186/s12936-018-2535-7
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