The impact of pollen consumption on honey bee digestive physiology and carbohydrate metabolism

Authors: Ricigliano, Vincent; FITZ, WILLIAM - University Of Arizona; Copeland, Duan; Mott, Brendon; MAES, PATRICK - University Of Arizona; Floyd, Amy; Dockstader, Arnold; Anderson, Kirk

Submitted to: Archives of Insect Biochemistry and Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/17/2017
Publication Date: 8/20/2017
Citation: Ricigliano, V.A., Fitz, W., Copeland, D.C., Mott, B.M., Maes, P., Floyd, A.S., Dockstader, A., Anderson, K.E. 2017. The impact of pollen consumption on honey bee digestive physiology and carbohydrate metabolism. Archives of Insect Biochemistry and Physiology. https://doi.org/10.1002/arch.21406.
DOI: https://doi.org/10.1002/arch.21406

Interpretive Summary: Pollen is the sole source of amino acids in the honey bee diet and its consumption and utilization have been investigated in considerable detail. Pollen is also a significant dietary source of carbohydrates, however non-starch carbohydrate metabolism in honey bees has been largely ignored by functional studies. Honey bees lack gene expression of certain carbohydrate active enzymes, specifically glycoside hydrolases (GHs) in gut tissues despite their reliance on a solely plant-based diet. This study highlights the functional roles of head gland secretions, gut microbiota and possibly pollen itself in non-starch carbohydrate metabolism in the honey bee. We found that pollen consumption stimulated the sugar-hydrolyzing potential of honey bee head and gut tissues, notably sugars that are toxic to the bee (xylose, arabinose, mannose). In vitro assays demonstrated the capacity of the bee gut microbiota to hydrolyze sugars from complex carbohydrates such as pectins and hemicelluloses and that pollen consumption by the bee alters bacterial abundance in gut tissues. Finally, we demonstrated that native enzyme activity in pollen itself may be sufficient for probable physiological activity in the gut. These findings are important to honey bee nutrition by the suggestion of additional roles for pollen in honey bee physiology beyond being a source of primary nutrients.

Technical Abstract: Carbohydrate-active enzymes play an important role in the honey bee (Apis mellifera) due to its dietary specialization on plant-based nutrition. Secretory glycoside hydrolases (GHs) produced in worker head glands aid in the processing of floral nectar into honey and are expressed in accordance with age-based division of labor. Pollen consumption and utilization by the honey bee have been investigated in considerable detail but little is known about the metabolic fate of indigestible pollen biomass. Here we demonstrate that pollen consumption stimulates the saccharification potential of native tissue homogenates, notably hydrolysis of sugars that are toxic to the bee (xylose, arabinose, mannose). GHs produced in the head accumulate in the midgut and persist in the hindgut which harbors a core microbial community comprised of approximately 108 bacterial cells. Pollen consumption significantly impacted total and specific bacterial abundance in the digestive tract. Bacterial isolates representing major fermentative gut phylotypes exhibited primarily membrane-bound GH activities that may function combinitorially with soluble host enzymes retained in the hindgut. Additionally, we found that plant-originating ß-galactosidase activity in vital pollen may be sufficient, in some cases, for probable physiological activity in the gut. These findings emphasize the potential relative contributions of host, bacteria, and dietary enzyme activities to total gut saccharolysis, which may be tied to gut microbiome dynamics and associated host nutrition.