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Transcriptomic, proteomic and ultrastructural studies on salinity-tolerant Aedes aegypti in the context of rising sea levels and arboviral disease epidemiology

BACKGROUND: Aedes aegypti mosquito, the principal global vector of arboviral diseases, lays eggs and undergoes larval and pupal development to become adult mosquitoes in fresh water (FW). It has recently been observed to develop in coastal brackish water (BW) habitats of up to 50% sea water, and suc...

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Autores principales: Ramasamy, Ranjan, Thiruchenthooran, Vaikunthavasan, Jayadas, Tibutius T. P., Eswaramohan, Thampoe, Santhirasegaram, Sharanga, Sivabalakrishnan, Kokila, Naguleswaran, Arunasalam, Uzest, Marilyne, Cayrol, Bastien, Voisin, Sebastien N., Bulet, Philippe, Surendran, Sinnathamby N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8034070/
https://www.ncbi.nlm.nih.gov/pubmed/33836668
http://dx.doi.org/10.1186/s12864-021-07564-8
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author Ramasamy, Ranjan
Thiruchenthooran, Vaikunthavasan
Jayadas, Tibutius T. P.
Eswaramohan, Thampoe
Santhirasegaram, Sharanga
Sivabalakrishnan, Kokila
Naguleswaran, Arunasalam
Uzest, Marilyne
Cayrol, Bastien
Voisin, Sebastien N.
Bulet, Philippe
Surendran, Sinnathamby N.
author_facet Ramasamy, Ranjan
Thiruchenthooran, Vaikunthavasan
Jayadas, Tibutius T. P.
Eswaramohan, Thampoe
Santhirasegaram, Sharanga
Sivabalakrishnan, Kokila
Naguleswaran, Arunasalam
Uzest, Marilyne
Cayrol, Bastien
Voisin, Sebastien N.
Bulet, Philippe
Surendran, Sinnathamby N.
author_sort Ramasamy, Ranjan
collection PubMed
description BACKGROUND: Aedes aegypti mosquito, the principal global vector of arboviral diseases, lays eggs and undergoes larval and pupal development to become adult mosquitoes in fresh water (FW). It has recently been observed to develop in coastal brackish water (BW) habitats of up to 50% sea water, and such salinity tolerance shown to be an inheritable trait. Genomics of salinity tolerance in Ae. aegypti has not been previously studied, but it is of fundamental biological interest and important for controlling arboviral diseases in the context of rising sea levels increasing coastal ground water salinity. RESULTS: BW- and FW-Ae. aegypti were compared by RNA-seq analysis on the gut, anal papillae and rest of the carcass in fourth instar larvae (L4), proteomics of cuticles shed when L4 metamorphose into pupae, and transmission electron microscopy of cuticles in L4 and adults. Genes for specific cuticle proteins, signalling proteins, moulting hormone-related proteins, membrane transporters, enzymes involved in cuticle metabolism, and cytochrome P450 showed different mRNA levels in BW and FW L4 tissues. The salinity-tolerant Ae. aegypti were also characterized by altered L4 cuticle proteomics and changes in cuticle ultrastructure of L4 and adults. CONCLUSIONS: The findings provide new information on molecular and ultrastructural changes associated with salinity adaptation in FW mosquitoes. Changes in cuticles of larvae and adults of salinity-tolerant Ae. aegypti are expected to reduce the efficacy of insecticides used for controlling arboviral diseases. Expansion of coastal BW habitats and their neglect for control measures facilitates the spread of salinity-tolerant Ae. aegypti and genes for salinity tolerance. The transmission of arboviral diseases can therefore be amplified in multiple ways by salinity-tolerant Ae. aegypti and requires appropriate mitigating measures. The findings in Ae. aegypti have attendant implications for the development of salinity tolerance in other fresh water mosquito vectors and the diseases they transmit. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07564-8.
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spelling pubmed-80340702021-04-12 Transcriptomic, proteomic and ultrastructural studies on salinity-tolerant Aedes aegypti in the context of rising sea levels and arboviral disease epidemiology Ramasamy, Ranjan Thiruchenthooran, Vaikunthavasan Jayadas, Tibutius T. P. Eswaramohan, Thampoe Santhirasegaram, Sharanga Sivabalakrishnan, Kokila Naguleswaran, Arunasalam Uzest, Marilyne Cayrol, Bastien Voisin, Sebastien N. Bulet, Philippe Surendran, Sinnathamby N. BMC Genomics Research Article BACKGROUND: Aedes aegypti mosquito, the principal global vector of arboviral diseases, lays eggs and undergoes larval and pupal development to become adult mosquitoes in fresh water (FW). It has recently been observed to develop in coastal brackish water (BW) habitats of up to 50% sea water, and such salinity tolerance shown to be an inheritable trait. Genomics of salinity tolerance in Ae. aegypti has not been previously studied, but it is of fundamental biological interest and important for controlling arboviral diseases in the context of rising sea levels increasing coastal ground water salinity. RESULTS: BW- and FW-Ae. aegypti were compared by RNA-seq analysis on the gut, anal papillae and rest of the carcass in fourth instar larvae (L4), proteomics of cuticles shed when L4 metamorphose into pupae, and transmission electron microscopy of cuticles in L4 and adults. Genes for specific cuticle proteins, signalling proteins, moulting hormone-related proteins, membrane transporters, enzymes involved in cuticle metabolism, and cytochrome P450 showed different mRNA levels in BW and FW L4 tissues. The salinity-tolerant Ae. aegypti were also characterized by altered L4 cuticle proteomics and changes in cuticle ultrastructure of L4 and adults. CONCLUSIONS: The findings provide new information on molecular and ultrastructural changes associated with salinity adaptation in FW mosquitoes. Changes in cuticles of larvae and adults of salinity-tolerant Ae. aegypti are expected to reduce the efficacy of insecticides used for controlling arboviral diseases. Expansion of coastal BW habitats and their neglect for control measures facilitates the spread of salinity-tolerant Ae. aegypti and genes for salinity tolerance. The transmission of arboviral diseases can therefore be amplified in multiple ways by salinity-tolerant Ae. aegypti and requires appropriate mitigating measures. The findings in Ae. aegypti have attendant implications for the development of salinity tolerance in other fresh water mosquito vectors and the diseases they transmit. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07564-8. BioMed Central 2021-04-09 /pmc/articles/PMC8034070/ /pubmed/33836668 http://dx.doi.org/10.1186/s12864-021-07564-8 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Ramasamy, Ranjan
Thiruchenthooran, Vaikunthavasan
Jayadas, Tibutius T. P.
Eswaramohan, Thampoe
Santhirasegaram, Sharanga
Sivabalakrishnan, Kokila
Naguleswaran, Arunasalam
Uzest, Marilyne
Cayrol, Bastien
Voisin, Sebastien N.
Bulet, Philippe
Surendran, Sinnathamby N.
Transcriptomic, proteomic and ultrastructural studies on salinity-tolerant Aedes aegypti in the context of rising sea levels and arboviral disease epidemiology
title Transcriptomic, proteomic and ultrastructural studies on salinity-tolerant Aedes aegypti in the context of rising sea levels and arboviral disease epidemiology
title_full Transcriptomic, proteomic and ultrastructural studies on salinity-tolerant Aedes aegypti in the context of rising sea levels and arboviral disease epidemiology
title_fullStr Transcriptomic, proteomic and ultrastructural studies on salinity-tolerant Aedes aegypti in the context of rising sea levels and arboviral disease epidemiology
title_full_unstemmed Transcriptomic, proteomic and ultrastructural studies on salinity-tolerant Aedes aegypti in the context of rising sea levels and arboviral disease epidemiology
title_short Transcriptomic, proteomic and ultrastructural studies on salinity-tolerant Aedes aegypti in the context of rising sea levels and arboviral disease epidemiology
title_sort transcriptomic, proteomic and ultrastructural studies on salinity-tolerant aedes aegypti in the context of rising sea levels and arboviral disease epidemiology
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8034070/
https://www.ncbi.nlm.nih.gov/pubmed/33836668
http://dx.doi.org/10.1186/s12864-021-07564-8
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