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Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal

SIMPLE SUMMARY: Female mosquitoes have been using the blood of their hosts to produce eggs for millions of years. As humans have become much more abundant in recent millennia, many mosquito species have adapted to bloodfeeding on humans, especially in drier areas where rehydration sources may not be...

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Autores principales: Holmes, Christopher J., Brown, Elliott S., Sharma, Dhriti, Warden, Matthew, Pathak, Atit, Payton, Blaine, Nguyen, Quynh, Spangler, Austin, Sivakumar, Jaishna, Hendershot, Jacob M., Benoit, Joshua B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10056721/
https://www.ncbi.nlm.nih.gov/pubmed/36975959
http://dx.doi.org/10.3390/insects14030274
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author Holmes, Christopher J.
Brown, Elliott S.
Sharma, Dhriti
Warden, Matthew
Pathak, Atit
Payton, Blaine
Nguyen, Quynh
Spangler, Austin
Sivakumar, Jaishna
Hendershot, Jacob M.
Benoit, Joshua B.
author_facet Holmes, Christopher J.
Brown, Elliott S.
Sharma, Dhriti
Warden, Matthew
Pathak, Atit
Payton, Blaine
Nguyen, Quynh
Spangler, Austin
Sivakumar, Jaishna
Hendershot, Jacob M.
Benoit, Joshua B.
author_sort Holmes, Christopher J.
collection PubMed
description SIMPLE SUMMARY: Female mosquitoes have been using the blood of their hosts to produce eggs for millions of years. As humans have become much more abundant in recent millennia, many mosquito species have adapted to bloodfeeding on humans, especially in drier areas where rehydration sources may not be as abundant. Some species, such as the yellow fever mosquito, Aedes aegypti, have even developed a distinct preference for human hosts. Unfortunately for us, these mosquitoes are also known to spread several pathogens during bloodfeeding, resulting in occurrences of yellow fever, dengue, Zika, chikungunya, as well as other diseases. Although decades of research have focused on these mosquitoes, more research is needed to understand how these mosquitoes are processing bloodmeals in the low humidity conditions where they often reside. In this study we examined the midgut of A. aegypti mosquitoes to determine how bloodmeal utilization changes after exposure to low humidity conditions and ultimately found that these mosquitoes can quickly and efficiently rehydrate through bloodfeeding. These results indicate that A. aegypti can rely on human bloodmeals to rehydrate in low humidity conditions when other resources may be scarce, potentially resulting in altered disease transmission rates. ABSTRACT: The mosquito midgut is an important site for bloodmeal regulation while also acting as a primary site for pathogen exposure within the mosquito. Recent studies show that exposure to dehydrating conditions alters mosquito bloodfeeding behaviors as well as post-feeding regulation, likely altering how pathogens interact with the mosquito. Unfortunately, few studies have explored the underlying dynamics between dehydration and bloodmeal utilization, and the overall impact on disease transmission dynamics remains veiled. In this study, we find that dehydration-based feeding in the yellow fever mosquito, Aedes aegypti, prompts alterations to midgut gene expression, as well as subsequent physiological factors involving water control and post-bloodfeeding (pbf) regulation. Altered expression of ion transporter genes and aquaporin 2 (AQP2) in the midgut of dehydrated mosquitoes as well as the rapid reequilibration of hemolymph osmolality after a bloodmeal indicate an ability to expedite fluid and ion processing. These alterations ultimately indicate that female A. aegypti employ mechanisms to ameliorate the detriments of dehydration by imbibing a bloodmeal, providing an effective avenue for rehydration. Continued research into bloodmeal utilization and the resulting effects on arthropod-borne transmission dynamics becomes increasingly important as drought prevalence is increased by climate change.
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spelling pubmed-100567212023-03-30 Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal Holmes, Christopher J. Brown, Elliott S. Sharma, Dhriti Warden, Matthew Pathak, Atit Payton, Blaine Nguyen, Quynh Spangler, Austin Sivakumar, Jaishna Hendershot, Jacob M. Benoit, Joshua B. Insects Article SIMPLE SUMMARY: Female mosquitoes have been using the blood of their hosts to produce eggs for millions of years. As humans have become much more abundant in recent millennia, many mosquito species have adapted to bloodfeeding on humans, especially in drier areas where rehydration sources may not be as abundant. Some species, such as the yellow fever mosquito, Aedes aegypti, have even developed a distinct preference for human hosts. Unfortunately for us, these mosquitoes are also known to spread several pathogens during bloodfeeding, resulting in occurrences of yellow fever, dengue, Zika, chikungunya, as well as other diseases. Although decades of research have focused on these mosquitoes, more research is needed to understand how these mosquitoes are processing bloodmeals in the low humidity conditions where they often reside. In this study we examined the midgut of A. aegypti mosquitoes to determine how bloodmeal utilization changes after exposure to low humidity conditions and ultimately found that these mosquitoes can quickly and efficiently rehydrate through bloodfeeding. These results indicate that A. aegypti can rely on human bloodmeals to rehydrate in low humidity conditions when other resources may be scarce, potentially resulting in altered disease transmission rates. ABSTRACT: The mosquito midgut is an important site for bloodmeal regulation while also acting as a primary site for pathogen exposure within the mosquito. Recent studies show that exposure to dehydrating conditions alters mosquito bloodfeeding behaviors as well as post-feeding regulation, likely altering how pathogens interact with the mosquito. Unfortunately, few studies have explored the underlying dynamics between dehydration and bloodmeal utilization, and the overall impact on disease transmission dynamics remains veiled. In this study, we find that dehydration-based feeding in the yellow fever mosquito, Aedes aegypti, prompts alterations to midgut gene expression, as well as subsequent physiological factors involving water control and post-bloodfeeding (pbf) regulation. Altered expression of ion transporter genes and aquaporin 2 (AQP2) in the midgut of dehydrated mosquitoes as well as the rapid reequilibration of hemolymph osmolality after a bloodmeal indicate an ability to expedite fluid and ion processing. These alterations ultimately indicate that female A. aegypti employ mechanisms to ameliorate the detriments of dehydration by imbibing a bloodmeal, providing an effective avenue for rehydration. Continued research into bloodmeal utilization and the resulting effects on arthropod-borne transmission dynamics becomes increasingly important as drought prevalence is increased by climate change. MDPI 2023-03-09 /pmc/articles/PMC10056721/ /pubmed/36975959 http://dx.doi.org/10.3390/insects14030274 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Holmes, Christopher J.
Brown, Elliott S.
Sharma, Dhriti
Warden, Matthew
Pathak, Atit
Payton, Blaine
Nguyen, Quynh
Spangler, Austin
Sivakumar, Jaishna
Hendershot, Jacob M.
Benoit, Joshua B.
Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal
title Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal
title_full Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal
title_fullStr Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal
title_full_unstemmed Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal
title_short Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal
title_sort dehydration alters transcript levels in the mosquito midgut, likely facilitating rapid rehydration following a bloodmeal
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10056721/
https://www.ncbi.nlm.nih.gov/pubmed/36975959
http://dx.doi.org/10.3390/insects14030274
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