Differential sensitivity and specificity of Aedes aegypti and Anopheles gambiae to adenine nucleotide phagostimulants—an all-or-none response?

Abstract Background The decision to imbibe a blood meal is predominantly dependent on the sensitivity and specificity of haematophagous arthropods to blood-derived adenine nucleotides, in particular adenosine triphosphate (ATP). Despite previous efforts to identify and characterise the specificity a...

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Main Authors: Matthew Lukenge, Rickard Ignell, Sharon Rose Hill
Format: Article
Language:English
Published: BMC 2024-11-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-024-06482-4
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author Matthew Lukenge
Rickard Ignell
Sharon Rose Hill
author_facet Matthew Lukenge
Rickard Ignell
Sharon Rose Hill
author_sort Matthew Lukenge
collection DOAJ
description Abstract Background The decision to imbibe a blood meal is predominantly dependent on the sensitivity and specificity of haematophagous arthropods to blood-derived adenine nucleotides, in particular adenosine triphosphate (ATP). Despite previous efforts to identify and characterise the specificity and sensitivity to ATP and other adenine nucleotides, as well as the role of other blood-derived phagostimulants across the Culicidae, comparisons across species remain difficult. Methods The feeding response of the yellow fever mosquito Aedes aegypti and the African malaria vector Anopheles gambiae to adenine nucleotides in the presence of a carbonate buffer was assessed using a membrane feeding assay. The proportion of mosquitoes engorged and the volume imbibed by all mosquitoes was scored visually and spectrophotometrically. In addition, the proportion of prediuresing An. gambiae, as well as the volume engorged and prediuresed, was examined. Results Aedes aegypti was more sensitive to adenine nucleotides than An. gambiae, but both species maintained specificity to these phagostimulants, demonstrating a dose-dependent bimodal feeding pattern, thereby expanding our understanding of the all-or-none blood-feeding hypothesis. Feeding on the bicarbonate buffer by An. gambiae—but not that of Ae. aegypti—demonstrated a species-specific variation in how blood phagostimulants are encoded. Adenine nucleotides, with and without bovine serum albumin, were observed to dose-dependently regulate the proportion of An. gambiae prediuresing and the volumes prediuresed but not volumes engorged. Conclusions Taken together, the results of this study expand our understanding of how mosquitoes differentially assess and respond to blood meal constituents, and provide a basis for further physiological and molecular studies. Graphical Abstract
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spelling doaj-art-a80f874d3fc349c9a012df65c9d6b70e2024-11-10T12:10:35ZengBMCParasites & Vectors1756-33052024-11-011711910.1186/s13071-024-06482-4Differential sensitivity and specificity of Aedes aegypti and Anopheles gambiae to adenine nucleotide phagostimulants—an all-or-none response?Matthew Lukenge0Rickard Ignell1Sharon Rose Hill2Disease Vector Group, Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural SciencesDisease Vector Group, Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural SciencesDisease Vector Group, Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural SciencesAbstract Background The decision to imbibe a blood meal is predominantly dependent on the sensitivity and specificity of haematophagous arthropods to blood-derived adenine nucleotides, in particular adenosine triphosphate (ATP). Despite previous efforts to identify and characterise the specificity and sensitivity to ATP and other adenine nucleotides, as well as the role of other blood-derived phagostimulants across the Culicidae, comparisons across species remain difficult. Methods The feeding response of the yellow fever mosquito Aedes aegypti and the African malaria vector Anopheles gambiae to adenine nucleotides in the presence of a carbonate buffer was assessed using a membrane feeding assay. The proportion of mosquitoes engorged and the volume imbibed by all mosquitoes was scored visually and spectrophotometrically. In addition, the proportion of prediuresing An. gambiae, as well as the volume engorged and prediuresed, was examined. Results Aedes aegypti was more sensitive to adenine nucleotides than An. gambiae, but both species maintained specificity to these phagostimulants, demonstrating a dose-dependent bimodal feeding pattern, thereby expanding our understanding of the all-or-none blood-feeding hypothesis. Feeding on the bicarbonate buffer by An. gambiae—but not that of Ae. aegypti—demonstrated a species-specific variation in how blood phagostimulants are encoded. Adenine nucleotides, with and without bovine serum albumin, were observed to dose-dependently regulate the proportion of An. gambiae prediuresing and the volumes prediuresed but not volumes engorged. Conclusions Taken together, the results of this study expand our understanding of how mosquitoes differentially assess and respond to blood meal constituents, and provide a basis for further physiological and molecular studies. Graphical Abstracthttps://doi.org/10.1186/s13071-024-06482-4Adenosine triphosphateBlood feedingMosquitoFeeding stimulantsPrediuresis
spellingShingle Matthew Lukenge
Rickard Ignell
Sharon Rose Hill
Differential sensitivity and specificity of Aedes aegypti and Anopheles gambiae to adenine nucleotide phagostimulants—an all-or-none response?
Parasites & Vectors
Adenosine triphosphate
Blood feeding
Mosquito
Feeding stimulants
Prediuresis
title Differential sensitivity and specificity of Aedes aegypti and Anopheles gambiae to adenine nucleotide phagostimulants—an all-or-none response?
title_full Differential sensitivity and specificity of Aedes aegypti and Anopheles gambiae to adenine nucleotide phagostimulants—an all-or-none response?
title_fullStr Differential sensitivity and specificity of Aedes aegypti and Anopheles gambiae to adenine nucleotide phagostimulants—an all-or-none response?
title_full_unstemmed Differential sensitivity and specificity of Aedes aegypti and Anopheles gambiae to adenine nucleotide phagostimulants—an all-or-none response?
title_short Differential sensitivity and specificity of Aedes aegypti and Anopheles gambiae to adenine nucleotide phagostimulants—an all-or-none response?
title_sort differential sensitivity and specificity of aedes aegypti and anopheles gambiae to adenine nucleotide phagostimulants an all or none response
topic Adenosine triphosphate
Blood feeding
Mosquito
Feeding stimulants
Prediuresis
url https://doi.org/10.1186/s13071-024-06482-4
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AT sharonrosehill differentialsensitivityandspecificityofaedesaegyptiandanophelesgambiaetoadeninenucleotidephagostimulantsanallornoneresponse