title: Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host.
abstract: Despite the demonstrated functional importance of gut microbes, our understanding of how animals regulate their metabolism in response to nutritionally 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. In line with bioassays demonstrating the symbionts' contribution towards host fitness through the supplementation of B vitamins, comparative transcriptomic analyses of genes involved in import and processing of B vitamins revealed an upregulation of gene expression in aposymbiotic (symbiont-free) compared with symbiotic individuals; an expression pattern that is indicative of B 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 the actinobacterial symbionts. Furthermore, the functional characterization of the differentially expressed thiamine transporter 2 through heterologous expression in Xenopus laevis oocytes confirms its role in cellular uptake of vitamin B1. These findings demonstrate that despite an extracellular localization, beneficial gut microbes can be integral to the host's metabolic homeostasis, reminiscent of bacteriome-localized intracellular mutualists.
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena 07745, Germany hsalem@ice.mpg.de.
authors.forename: Hassan
authors.initials: H
authors.lastname: Salem
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena 07745, Germany.
authors.forename: Eugen
authors.initials: E
authors.lastname: Bauer
authors.affiliation: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena 07745, Germany.
authors.forename: Anja S
authors.initials: AS
authors.lastname: Strauss
authors.affiliation: Department of Entomology, Max Planck Institute for Chemical Ecology, Jena 07745, Germany.
authors.forename: Heiko
authors.initials: H
authors.lastname: Vogel
authors.affiliation: Faculty of Mathematics and Computer Science, Friedrich Schiller University, Jena 07743, Germany.
authors.forename: Manja
authors.initials: M
authors.lastname: Marz
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena 07745, Germany mkaltenpoth@ice.mpg.de.
authors.forename: Martin
authors.initials: M
authors.lastname: Kaltenpoth
mesh_terms: D039903:Actinobacteria / Q000378:metabolism / Q000502:physiology*; D000824:Animal Nutritional Physiological Phenomena; D000818:Animals; D001692:Biological Transport; D020062:Heteroptera / Q000235:genetics / Q000378:metabolism / Q000382:microbiology*; D006706:Homeostasis; D053858:Metabolic Networks and Pathways; D013559:Symbiosis; D059467:Transcriptome; D014803:Vitamin B Complex / Q000096:biosynthesis; D014815:Vitamins / Q000378:metabolism*; D014982:Xenopus laevis
chemical_list: D014815:Vitamins; D014803:Vitamin B Complex
keywords: host–microbe metabolic integration; mutualism; nutritional symbiosis; symbiont transmission; vitamin supplementation