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.

Symbiont transmission entails the risk of parasite infection

“…Transcriptome sequencing of poly-A enriched mRNAs, assembly, annotation and analysis were described previously [9,20]. The sequence data were deposited in the European Nucleotide Archive, accession number PRJEB6171 (http://www.ebi.ac.uk/ena/data/view/PRJEB6171).…”

“…are vertically transmitted across host generations through the faecal smearing of egg surfaces by females during oviposition, but can also be horizontally acquired through contact with conspecifics [7]. Experimental sterilization of egg surfaces disrupts the transmission cycle of the Coriobacteriaceae symbionts, resulting in aposymbiotic (symbiont-free) firebugs that suffer retarded growth, high mortality and low fecundity [8], which is owing to the deficiency in B vitamins that are provided by the symbionts [9].…”

“…The four treatments were provided ad libitum with autoclaved water and a nutrient-rich artificial diet [9].…”

An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects

“…Such experiments have been successfully employed to elucidate symbiont contributions towards host fitness, to assess host-symbiont specificity, and to detail the effects of symbiont replacement on host ecology (e.g. [66,67]). …”

Culturing and Characterization of Gut Symbiont Burkholderia spp. from the Southern Chinch Bug, Blissus insularis (Hemiptera: Blissidae)

“…These symbionts usually colonize specialized regions of the midgut, are transmitted to offspring by egg smearing, symbiont-containing capsules, or coprophagy, and play a role in host insect fitness (3)(4)(5)(6)(7). Exocellular symbionts can provide nutrients to supplement the unbalanced diets of their host insects (1,(8)(9)(10))m thus conferring fitness advantages (e.g., body size, coloration, development, and growth) (11)(12)(13). In addition, these symbionts have been reported to elicit symbiont-mediated plant specialization (14), to modulate plant virus transmission (15,16), and/or to induce protection against pathogenic gut bacteria (17), protozoan parasites (18), and synthetic insecticides (19).…”