Vitamin Supplementation by Gut Symbionts Ensures Metabolic Homeostasis in an Insect Host

Many animals are dependent on intestinal microbes for nutrition. However, our understanding of how the host regulates its metabolism in response to beneficial symbionts remains limited. Here we elucidate the functional importance of the African cotton stainer’s (Dysdercus fasciatus) association with two actinobacterial gut symbionts and subsequently examine the insect’s transcriptional response following symbiont elimination. Genomic analyses and bioassays demonstrate the symbionts’ contribution towards host fitness through the supplementation of B vitamins. Concordantly, comparative transcriptomic analyses reveal a differential up-regulation of genes involved in import and processing of B vitamins in aposymbiotic bugs; an expression pattern that is indicative of vitamin deficiency in animals. Normal expression levels of these genes, however, can be restored by either artificial supplementation of B vitamins into the insect’s diet or reinfection with actinobacterial symbionts. Furthermore, the functional characterization of the differentially expressed thiamine transporter 2 (THTR2) through heterologous expression in Xenopus laevis oocytes confirms its role in cellular uptake of vitamin B1. Taken together, our findings demonstrate that – despite an extracellular localization – beneficial gut microbes can be integral to an insect’s metabolic homeostasis, reminiscent of bacteriome-localized intracellular mutualists.