Immunometabolism in Arthropod Vectors: Redefining Interspecies Relationships

Abstract

Metabolism influences biochemical networks and arthropod vectors are endowed with an immune system that affects microbial acquisition, persistence and transmission to humans and other animals. Here, we aim to persuade the scientific community to expand their interests in immunometabolism beyond mammalian hosts and towards arthropod vectors. Immunometabolism investigates the interplay of metabolism and immunology. We provide a conceptual framework for investigators from diverse disciplines and indicate that relationships between microbes, mammalian hosts and their hematophagous arthropods may result in cost-effective (mutualism) or energetically expensive (parasitism) interactions. We argue that disparate resource allocations between species may partially explain why some microbes act as pathogens when infecting humans and behave as mutualistic or commensal organisms when colonizing arthropod vectors.

Trained Immunity in Anopheles gambiae: Antibacterial Immunity Is Enhanced by Priming via Sugar Meal Supplemented With a Single Gut Symbiotic Bacterial Strain

“…Increasing evidence has emerged that solute carrier transporters play critical roles in nutrient uptake, ion influx/efflux, and waste disposal, which mediates energy and metabolic support for immune activities (Song et al, 2020). Further study is needed to explore the priming effect on immunometabolism, which has become a hot research area recently (Penkov et al, 2019;Samaddar et al, 2020).…”

Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection

“…Malaria remains a deadly disease, which is best combatted by controlling mosquito populations [61,62]. A variety of approaches are currently being undertaken with this goal [1][2][3][4][5][6][7][8]. We propose that metal chelators offer an additional tool that is worth considering in vector-borne disease control programs and potentially also in the control or monitoring of fruit flies of economic impotance [80].…”

“…Many strategies have been applied for vector control [2], with recent additions including genetic strategies [3,4], manipulation of the Wolbachia endosymbiont [5], and proposals to influence mosquito behavior [6]. A thorough characterization of the physiological interactions between viruses or parasites and their insect hosts could further inform the design of interventions to interrupt infections in affected areas [7,8]. One such relatively unexplored area of insect physiology-with the possible exception of studies in the model organism Drosophila melanogaster [9][10][11][12][13]-is metal metabolism.…”

Non-immune Traits Triggered by Blood Intake Impact Vectorial Competence

“…Sugar metabolism in these animals is controlled at the hormonal level by ILP and juvenile hormone (JH) (Clifton and Noriega, 2011;Hansen et al, 2014;Hou et al, 2015;Roy et al, 2015). It is increasingly clear that parasites can dramatically change the cellular energy metabolism of their arthropod vectors, as recently revised by Samaddar et al (2020). Still, for mosquito-arbovirus interactions, the knowledge on such metabolic alterations is limited.…”

“…However, the relevance of these changes to the course of viral infection has not been experimentally addressed in the literature yet, despite alterations in expression of metabolic enzymes being regularly observed in transcriptomic analyses of infected vector digestive apparatus (Padrón et al, 2014;Angleró-Rodríguez et al, 2017a;Etebari et al, 2017;Narasimhan et al, 2017;Coutinho-Abreu et al, 2020). A large amount of gene expression data on vector infection has now accumulated, and it could be used to direct studies focusing on the crosstalk between canonical immunity pathways and carbohydrate/energy metabolism, the so-called immunometabolism, and the relevance of them to vector biology (Samaddar et al, 2020).…”