Changes in Microbiota Across Developmental Stages of Aedes koreicus, an Invasive Mosquito Vector in Europe: Indications for Microbiota-Based Control Strategies

Since it has been understood that gut microbiota of vector mosquitoes can influence their vector competence, efforts have been undertaken to develop new control strategies based on host microbiota manipulation, and aimed at suppressing the vector population or replacing it with a less competent one....

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Main Authors: Niccolò Alfano, Valentina Tagliapietra, Fausta Rosso, Mattia Manica, Daniele Arnoldi, Massimo Pindo, Annapaola Rizzoli
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02832/full
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spelling doaj-cc681713bfb24ac8801efefa215a9eed2020-11-25T00:53:44ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-12-011010.3389/fmicb.2019.02832493957Changes in Microbiota Across Developmental Stages of Aedes koreicus, an Invasive Mosquito Vector in Europe: Indications for Microbiota-Based Control StrategiesNiccolò AlfanoValentina TagliapietraFausta RossoMattia ManicaDaniele ArnoldiMassimo PindoAnnapaola RizzoliSince it has been understood that gut microbiota of vector mosquitoes can influence their vector competence, efforts have been undertaken to develop new control strategies based on host microbiota manipulation, and aimed at suppressing the vector population or replacing it with a less competent one. For the proper design of such control strategies it is necessary to know the microbiota composition of the target vector species, how it is acquired, and how it changes throughout the host’s life cycle. In this study, 16S rRNA amplicon high-throughput sequencing was used to characterize the changes in microbiota from the aquatic environment (larval breeding sites) to the different developmental stages of field-collected Aedes koreicus in Italy, an emerging invasive mosquito species in Europe and a potential vector of several pathogens. The bacterial communities of the aquatic breeding sites, larvae, pupae and adults showed distinctive structures to one another. Indeed, 84% of community members were unique to a given sample type. Nevertheless, almost 40% of the sequences generated were assigned to bacteria detected in all sample types, suggesting the importance of bacteria transstadially transmitted from water to the adult stage in constituting mosquito microbiota. Among these, genus C39 largely constituted water microbiota, family Burkholderiaceae was the most abundant in larvae and pupae, and genus Asaia dominated adult communities. In addition, Asaia constituted a core microbiota across all sample types. Our results suggest that the microbiota of Ae. koreicus mosquitoes is composed by a community which derives from the aquatic bacteria of the larval breeding sites, is then filtered by the larval gut, where only certain members are able to persist, rearranged by metamorphosis and finally modified by the change in diet at the adult stage. Understanding how the microbiota of Ae. koreicus changes through the mosquito life cycle represents a first step in selecting bacterial candidates for use in microbiota-based intervention measures for this species. The properties which Asaia exhibits in this species, such as dominance, high prevalence and transstadial transmission, prevent the use of Wolbachia but make Asaia an ideal candidate for paratransgenesis.https://www.frontiersin.org/article/10.3389/fmicb.2019.02832/fullAedes koreicusmicrobiotadevelopmental stageslarval habitatsvector controltransstadial transmission
collection DOAJ
language English
format Article
sources DOAJ
author Niccolò Alfano
Valentina Tagliapietra
Fausta Rosso
Mattia Manica
Daniele Arnoldi
Massimo Pindo
Annapaola Rizzoli
spellingShingle Niccolò Alfano
Valentina Tagliapietra
Fausta Rosso
Mattia Manica
Daniele Arnoldi
Massimo Pindo
Annapaola Rizzoli
Changes in Microbiota Across Developmental Stages of Aedes koreicus, an Invasive Mosquito Vector in Europe: Indications for Microbiota-Based Control Strategies
Frontiers in Microbiology
Aedes koreicus
microbiota
developmental stages
larval habitats
vector control
transstadial transmission
author_facet Niccolò Alfano
Valentina Tagliapietra
Fausta Rosso
Mattia Manica
Daniele Arnoldi
Massimo Pindo
Annapaola Rizzoli
author_sort Niccolò Alfano
title Changes in Microbiota Across Developmental Stages of Aedes koreicus, an Invasive Mosquito Vector in Europe: Indications for Microbiota-Based Control Strategies
title_short Changes in Microbiota Across Developmental Stages of Aedes koreicus, an Invasive Mosquito Vector in Europe: Indications for Microbiota-Based Control Strategies
title_full Changes in Microbiota Across Developmental Stages of Aedes koreicus, an Invasive Mosquito Vector in Europe: Indications for Microbiota-Based Control Strategies
title_fullStr Changes in Microbiota Across Developmental Stages of Aedes koreicus, an Invasive Mosquito Vector in Europe: Indications for Microbiota-Based Control Strategies
title_full_unstemmed Changes in Microbiota Across Developmental Stages of Aedes koreicus, an Invasive Mosquito Vector in Europe: Indications for Microbiota-Based Control Strategies
title_sort changes in microbiota across developmental stages of aedes koreicus, an invasive mosquito vector in europe: indications for microbiota-based control strategies
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-12-01
description Since it has been understood that gut microbiota of vector mosquitoes can influence their vector competence, efforts have been undertaken to develop new control strategies based on host microbiota manipulation, and aimed at suppressing the vector population or replacing it with a less competent one. For the proper design of such control strategies it is necessary to know the microbiota composition of the target vector species, how it is acquired, and how it changes throughout the host’s life cycle. In this study, 16S rRNA amplicon high-throughput sequencing was used to characterize the changes in microbiota from the aquatic environment (larval breeding sites) to the different developmental stages of field-collected Aedes koreicus in Italy, an emerging invasive mosquito species in Europe and a potential vector of several pathogens. The bacterial communities of the aquatic breeding sites, larvae, pupae and adults showed distinctive structures to one another. Indeed, 84% of community members were unique to a given sample type. Nevertheless, almost 40% of the sequences generated were assigned to bacteria detected in all sample types, suggesting the importance of bacteria transstadially transmitted from water to the adult stage in constituting mosquito microbiota. Among these, genus C39 largely constituted water microbiota, family Burkholderiaceae was the most abundant in larvae and pupae, and genus Asaia dominated adult communities. In addition, Asaia constituted a core microbiota across all sample types. Our results suggest that the microbiota of Ae. koreicus mosquitoes is composed by a community which derives from the aquatic bacteria of the larval breeding sites, is then filtered by the larval gut, where only certain members are able to persist, rearranged by metamorphosis and finally modified by the change in diet at the adult stage. Understanding how the microbiota of Ae. koreicus changes through the mosquito life cycle represents a first step in selecting bacterial candidates for use in microbiota-based intervention measures for this species. The properties which Asaia exhibits in this species, such as dominance, high prevalence and transstadial transmission, prevent the use of Wolbachia but make Asaia an ideal candidate for paratransgenesis.
topic Aedes koreicus
microbiota
developmental stages
larval habitats
vector control
transstadial transmission
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02832/full
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