Probing the honey bee diet-microbiota-host axis using pollen restriction and organic acid feeding

Authors: Ricigliano, Vincent; Anderson, Kirk

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/7/2020
Publication Date: 5/9/2020
Citation: Ricigliano, V.A., Anderson, K.E. 2020. Probing the honey bee diet-microbiota-host axis using pollen restriction and organic acid feeding. Insects. 11(5):1-14. https://doi.org/10.3390/insects11050291.
DOI: https://doi.org/10.3390/insects11050291

Interpretive Summary: Honey bees harbor a gut microbiota with putative nutritive functions although there is limited understanding as to how it interacts with diet to influence the bee host. In this study, we describe a previously uncharacterized bacterial community in the honey bee anterior rectum. Using simple diet manipulations of pollen restriction and organic acid feeding, we quantified the role of pollen as a microbiota growth substrate as well as the influence of bacterial fermentation products on gut hormone signaling. Dietary pollen restriction markedly reduced total and specific bacterial abundance in the anterior rectum but not the ileum. The expression of bacterial fermentative metabolic genes was reduced in association with diet-induced microbiota shifts. Feeding bees organic acids significantly impacted gut hormone (enteroendocrine) signaling gene expression. This was specifically manifested by tissue-dependent expression patterns of neuropeptide F and allatostatin pathways, which are implicated in energy metabolism and feeding behaviors. Our findings provide new insights into interactions between diet, microbiota, and host physiology in honey bees and may inform future efforts to improve bee health through diet-based microbiota.

Technical Abstract: Microbial metabolites are considered important drivers of diet-based microbiota influence on the host, however mechanistic models are confounded by interactions between diet, microbiota function, and host physiology. The honey bee harbors a simple microbiota that produces organic acids as fermentation products of dietary nectar and pollen, making it a model for gut microbiota research. Here, we describe a large bacterial community and putative host-microbe nutrition interface in the bee anterior rectum. The role of undigested pollen as a microbiota growth substrate was quantified via expression profiling of bacterial 16S rRNAs and metabolic genes in vivo. Dietary pollen restriction markedly reduced total and specific bacterial abundance in the anterior rectum but not in the ileum. Anterior rectum expression levels of fermentative enzyme gene transcripts (acetate kinase, lactate dehydrogenase, and hydroxybutyryl-CoA dehydrogenase) were reduced in association with diet-induced microbiota shifts. To evaluate the effects of fermentative metabolites on host enteroendocrine function, pollen-restricted bees were fed an equimolar mixture of organic acid sodium salts (acetate, lactate, butyrate, formate and succinate). Organic acid feeding significantly impacted hindgut enteroendocrine signaling gene expression, rescuing some effects of pollen restriction. This was specifically manifested by tissue-dependent expression patterns of neuropeptide F and allatostatin pathways, which are implicated in energy metabolism and feeding behaviors. Our findings provide new insights into the diet-microbiota-host axis in honey bees and may inform future efforts to improve bee health through diet-based microbiota manipulations.