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Bidirectional Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch-Associated Responses in the Mosquito Anopheles culicifacies

The periodic ingestion of a protein-rich blood meal by adult female mosquitoes causes a drastic metabolic change in their innate physiological status, which is referred to as a ‘metabolic switch’. While understanding the neural circuits for host-seeking is modestly attended, how the gut ‘metabolic s...

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Autores principales: Das De, Tanwee, Sharma, Punita, Tevatiya, Sanjay, Chauhan, Charu, Kumari, Seena, Yadav, Pooja, Singla, Deepak, Srivastava, Vartika, Rani, Jyoti, Hasija, Yasha, Pandey, Kailash C., Kajla, Mayur, Dixit, Rajnikant
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9180301/
https://www.ncbi.nlm.nih.gov/pubmed/35681493
http://dx.doi.org/10.3390/cells11111798
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author Das De, Tanwee
Sharma, Punita
Tevatiya, Sanjay
Chauhan, Charu
Kumari, Seena
Yadav, Pooja
Singla, Deepak
Srivastava, Vartika
Rani, Jyoti
Hasija, Yasha
Pandey, Kailash C.
Kajla, Mayur
Dixit, Rajnikant
author_facet Das De, Tanwee
Sharma, Punita
Tevatiya, Sanjay
Chauhan, Charu
Kumari, Seena
Yadav, Pooja
Singla, Deepak
Srivastava, Vartika
Rani, Jyoti
Hasija, Yasha
Pandey, Kailash C.
Kajla, Mayur
Dixit, Rajnikant
author_sort Das De, Tanwee
collection PubMed
description The periodic ingestion of a protein-rich blood meal by adult female mosquitoes causes a drastic metabolic change in their innate physiological status, which is referred to as a ‘metabolic switch’. While understanding the neural circuits for host-seeking is modestly attended, how the gut ‘metabolic switch’ modulates brain functions, and resilience to physiological homeostasis, remains unexplored. Here, through a comparative brain RNA-Seq study, we demonstrate that the protein-rich diet induces the expression of brain transcripts related to mitochondrial function and energy metabolism, possibly causing a shift in the brain’s engagement to manage organismal homeostasis. A dynamic mRNA expression pattern of neuro-signaling and neuro-modulatory genes in both the gut and brain likely establishes an active gut–brain communication. The disruption of this communication through decapitation does not affect the modulation of the neuro-modulator receptor genes in the gut. In parallel, an unusual and paramount shift in the level of neurotransmitters (NTs), from the brain to the gut after blood feeding, further supports the idea of the gut’s ability to serve as a ‘second brain’. After blood-feeding, a moderate enrichment of the gut microbial population, and altered immunity in the gut of histamine receptor-silenced mosquitoes, provide initial evidence that the gut-microbiome plays a crucial role in gut–brain–axis communication. Finally, a comparative metagenomics evaluation of the gut microbiome highlighted that blood-feeding enriches the family members of the Morganellaceae and Pseudomonadaceae bacterial communities. The notable observation of a rapid proliferation of Pseudomonas bacterial sp. and tryptophan enrichment in the gut correlates with the suppression of appetite after blood-feeding. Additionally, altered NTs dynamics of naïve and aseptic mosquitoes provide further evidence that gut-endosymbionts are key modulators for the synthesis of major neuroactive molecules. Our data establish a new conceptual understanding of microbiome–gut–brain–axis communication in mosquitoes.
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spelling pubmed-91803012022-06-10 Bidirectional Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch-Associated Responses in the Mosquito Anopheles culicifacies Das De, Tanwee Sharma, Punita Tevatiya, Sanjay Chauhan, Charu Kumari, Seena Yadav, Pooja Singla, Deepak Srivastava, Vartika Rani, Jyoti Hasija, Yasha Pandey, Kailash C. Kajla, Mayur Dixit, Rajnikant Cells Article The periodic ingestion of a protein-rich blood meal by adult female mosquitoes causes a drastic metabolic change in their innate physiological status, which is referred to as a ‘metabolic switch’. While understanding the neural circuits for host-seeking is modestly attended, how the gut ‘metabolic switch’ modulates brain functions, and resilience to physiological homeostasis, remains unexplored. Here, through a comparative brain RNA-Seq study, we demonstrate that the protein-rich diet induces the expression of brain transcripts related to mitochondrial function and energy metabolism, possibly causing a shift in the brain’s engagement to manage organismal homeostasis. A dynamic mRNA expression pattern of neuro-signaling and neuro-modulatory genes in both the gut and brain likely establishes an active gut–brain communication. The disruption of this communication through decapitation does not affect the modulation of the neuro-modulator receptor genes in the gut. In parallel, an unusual and paramount shift in the level of neurotransmitters (NTs), from the brain to the gut after blood feeding, further supports the idea of the gut’s ability to serve as a ‘second brain’. After blood-feeding, a moderate enrichment of the gut microbial population, and altered immunity in the gut of histamine receptor-silenced mosquitoes, provide initial evidence that the gut-microbiome plays a crucial role in gut–brain–axis communication. Finally, a comparative metagenomics evaluation of the gut microbiome highlighted that blood-feeding enriches the family members of the Morganellaceae and Pseudomonadaceae bacterial communities. The notable observation of a rapid proliferation of Pseudomonas bacterial sp. and tryptophan enrichment in the gut correlates with the suppression of appetite after blood-feeding. Additionally, altered NTs dynamics of naïve and aseptic mosquitoes provide further evidence that gut-endosymbionts are key modulators for the synthesis of major neuroactive molecules. Our data establish a new conceptual understanding of microbiome–gut–brain–axis communication in mosquitoes. MDPI 2022-05-31 /pmc/articles/PMC9180301/ /pubmed/35681493 http://dx.doi.org/10.3390/cells11111798 Text en © 2022 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
Das De, Tanwee
Sharma, Punita
Tevatiya, Sanjay
Chauhan, Charu
Kumari, Seena
Yadav, Pooja
Singla, Deepak
Srivastava, Vartika
Rani, Jyoti
Hasija, Yasha
Pandey, Kailash C.
Kajla, Mayur
Dixit, Rajnikant
Bidirectional Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch-Associated Responses in the Mosquito Anopheles culicifacies
title Bidirectional Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch-Associated Responses in the Mosquito Anopheles culicifacies
title_full Bidirectional Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch-Associated Responses in the Mosquito Anopheles culicifacies
title_fullStr Bidirectional Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch-Associated Responses in the Mosquito Anopheles culicifacies
title_full_unstemmed Bidirectional Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch-Associated Responses in the Mosquito Anopheles culicifacies
title_short Bidirectional Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch-Associated Responses in the Mosquito Anopheles culicifacies
title_sort bidirectional microbiome-gut-brain-axis communication influences metabolic switch-associated responses in the mosquito anopheles culicifacies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9180301/
https://www.ncbi.nlm.nih.gov/pubmed/35681493
http://dx.doi.org/10.3390/cells11111798
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