Diet-related gut bacterial dysbiosis correlates with impaired development and increased mortality in the honey bee (Apis mellifera)

Authors: MAES, PATRICK - University Of Arizona; RODRIGUES, PEDRO - University Of Arizona; OLIVER, RANDY - Non ARS Employee; Mott, Brendon; Anderson, Kirk

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/26/2016
Publication Date: 10/27/2016
Citation: Maes, P., Rodrigues, P., Oliver, R., Mott, B.M., Anderson, K.E. 2016. Diet-related gut bacterial dysbiosis correlates with impaired development and increased mortality in the honey bee (Apis mellifera). Molecular Ecology. 25(21):5439-5450. https://doi.org/10.1111/mec.13862.
DOI: https://doi.org/10.1111/mec.13862

Interpretive Summary: Bacteria in the guts of animals often play critical roles in health. The change in bacterial species in the gut can be associated with a variety of disease states. Here we determined the effect of nutrient source on gut bacterial composition of the honey bee (Apis mellifera). We provided caged bees with naturally collected pollen and pollen substitute, both fresh and aged, then recorded host development and bacterial community composition of four nutrient-processing host tissues. Feeding fresh pollen or fresh substitute, we found no difference in host mortality, consumption rate, development, or bacterial species. In contrast, bees fed an aged diet differed markedly from those fed fresh diet, suffered impaired development and increased mortality, and developed a significantly different bacterial species composition throughout the gut. Consumption of an aged diet resulted in a significant reduction of the hindgut bacterium Snodgrassella alvi and a corresponding increase of opportunistic pathogen Frischella perrara. Moreover, the relative abundance of S. alvi in the hindgut was positively correlated with host survival and development. The inverse was true for F. perrara, reinforcing its role as an opportunistic gut pathogen. Echoing results from bumble bees, Parasacharibacter apium was also associated with negative host effects in general. Collectively, our findings suggest that the early establishment of S. alvi is associated with healthy nurse development, due to the exclusion of F. perrara and P. apium from the hindgut. Our findings provide insight into the role nutrition plays in host health and the establishment of characeristic gut bacteria.

Technical Abstract: Dysbiosis, defined as unhealthy shifts in bacterial community composition, can lower the colonization resistance of the gut to intrinsic pathogens. Here, we determined the effect of diet age and type on the health and bacterial community composition of the honeybee (Apis mellifera). We fed newly emerged bees fresh or aged diets, and then recorded host development and bacterial community composition from four distinct regions of the hosts’ digestive tract. Feeding fresh pollen or fresh substitute, we found no difference in host mortality, diet consumption, development or microbial community composition. In contrast, bees fed aged diets suffered impaired development, increased mortality and developed a significantly dysbiotic microbiome. The consumption of aged diets resulted in a significant reduction in the core ileum bacterium Snodgrassella alvi and a corresponding increase in intrinsic pathogen Frischella perrara. Moreover, the relative abundance of S. alvi in the ileum was positively correlated with host survival and development. The inverse was true for both F. perrara and Parasacharibacter apium. Collectively, our findings suggest that the early establishment of S. alvi is associated with healthy nurse development and potentially excludes F. perrara and P. apium from the ileum. Although at low abundance, establishment of the common midgut pathogen Nosema spp. was significantly associated with ileum dysbiosis and associated host deficiencies. Moreover, dysbiosis in the ileum was reflected in the rectum, mouthparts and hypopharyngeal glands, suggesting a systemic host effect. Our findings demonstrate that typically occurring alterations in diet quality play a significant role in colony health and the establishment of a dysbiotic gut microbiome.