Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch in the Mosquito Anopheles Culicifacies

Abstract

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 ‘metabolic switch. Although the down-regulation of olfactory factors is key to restrain host-attraction, how the gut ‘metabolic switch’ modulates brain functions, and resilience physiological homeostasis remains unexplored. Here we demonstrate that the protein-rich diet induces the expression of brain transcripts related to mitochondrial function and energy metabolism, possibly to cause a shift of the brain’s engagement to manage organismal homeostasis. A dynamic expression pattern of neuro-signalling and neuro-modulatory genes in both gut and brain, establishes an active brain-distant organ communication. Disruption of this comunication 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 the 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’. Finally, a comparative metagenomics evaluation of gut microbiome population dynamics, highlighted that blood-feeding not only suppresses Enterobacteriaceae family member by 50%, but favors rapid proliferation of Pseudomonadales to 46% of the total community. Notable obesrvation of a rapid proliferation of Pseudomonas bacterial sp. in the gut correlates a possible cause for the suppression of appetite after blood-feeding. Additionally, an altered NTs dynamics of naïve and aseptic mosquitoes provide the initial evidence that gut-endosymbionts are key modulators for the synthesis of major neuroactive molecules. Conclusion: Our data establish a new conceptual understanding of microbiome-gut-brain-axis communication in mosquitoes.Data deposition: Mosquito Brain RNAseq data are accessible under Accession IDs: SRR9853884 (Ac-Br-SF); SRR9853885 (Ac-Br-BF-30Min), SRR9853883 (Ac-Br-BF-30hrs) at NCBI repository. Mosquito Gut metagenomics data are accessible under accession IDs: SRR12579422 (Ac-MG-SF); SRR12622557 (Ac-MG-BF) at NCBI repository.