Grandeur Alliances: Symbiont Metabolic Integration and Obligate Arthropod Hematophagy

Abstract

Several arthropod taxa live exclusively on vertebrate blood. This food source lacks essential metabolites required for the maintenance of metabolic homeostasis, and as such, these arthropods have formed symbioses with nutrient-supplementing microbes that facilitate their host's 'hematophagous' feeding ecology. Herein we highlight metabolic contributions of bacterial symbionts that reside within tsetse flies, bed bugs, lice, reduviid bugs, and ticks, with specific emphasis on B vitamin and cofactor biosynthesis. Importantly, these arthropods can transmit pathogens of medical and veterinary relevance and/or cause infestations that induce psychological and dermatological distress. Microbial metabolites, and the biochemical pathways that generate them, can serve as specific targets of novel control mechanisms aimed at disrupting the metabolism of hematophagous arthropods, thus combatting pest invasion and vector-borne pathogen transmission.

Keywords: B vitamins; blood; hematophagy; microbiota; symbiont; vector.

Figure 1. Symbiont nutrient complementation in tsetse flies and bed bugs

Tsetse’s obligate symbiont, Wigglesworthia, is found within bacteriocytes in adult and larval stage flies. Sodalis, tsetse’s commensal symbiont, exhibits a broad tissue tropism and is found intra- and extracellularly in many host tissues. Extracellular populations of Wigglesworthia and Sodalis are transmitted to developing intrauterine larvae via maternal milk gland secretions. Wigglesworthia-provisioned metabolites are secreted from tsetse’s bacteriome into the hemolymph, from which they are taken up by the female’s fat body and milk gland for energy production and larval uptake. Sodalis also scavenges thiamine produced by Wigglesworthia. Bed bugs have entered into an obligate symbiosis with the bacterium Wolbachia (strain wCle). wCle resides within a pair of bacteriomes immediately adjacent to the bed bug’s gonads, thus facilitating vertical transmission. When treated with antibiotics to eliminate their obligate symbionts, both tsetse flies and bed bugs exhibit impaired development and reproductive sterility.