Social microbiota and social gland gene expression of worker honey bees by age and climate

Authors: Anderson, Kirk; MAES, P. - University Of Arizona

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/7/2022
Publication Date: 6/23/2022
Citation: Anderson, K.E., Maes, P. 2022. Social microbiota and social gland gene expression of worker honey bees by age and climate. Scientific Reports. 12. Article 10690. https://doi.org/10.1038/s41598-022-14442-0.
DOI: https://doi.org/10.1038/s41598-022-14442-0

Interpretive Summary: Overwintering is a major contributor to honey bee colony loss worldwide and is hypothesized to involve changes in colony physiology and behavior that render individuals more susceptible to disease. Here we DNA sequence the microbes associated with stored food, mouthparts and midguts of honey bees before and after winter from both warm and cold overwintering climates. We hypothesized that fluctuations in temperature and water availability may affect microbial character producing an environment conducive to the growth of opportunists. We detail the change in immune gene expression in the hypopharygeal gland overwinter, a secretory gland that interfaces with the extended social environment on many levels. We found major differences in the microbiome of stored pollen overwinter. The cold, controlled overwintering environment produced the healthiest result based on immune gene expression, and microbiome characteristics. Warm overwintering was associated changes in the midgut and mouthpart microbiota that suggest increased disease susceptibility, including significantly greater abundance of opportunistic bacteria in the worker midgut post-winter. Concurrently, the significant reduction in opportunistic bacteria on the mouthparts of the same bees showing significantly greater immune gene expression in their salivary glands, and increased opportunistic bacteria in their midguts suggests a hygienic response to hive opportunists overwinter. In general, we found many differences in microbiome structure between warm and cold overwintering environments. Our results may reflect selection pressures that shaped the social and hive microbiome with evolution to a perennial life history.

Technical Abstract: Overwintering is a major contributor to honey bee colony loss worldwide and is hypothesized to involve changes in colony physiology and behavior that render indiv iduals more susceptible to disease. Here we investigate the microbial niche space of the hive overwinter, sequencing the microbiomes of stored food, mouthparts and midguts of honey bees before and after winter from both warm and cold overwintering climates. We hypothesized that fluctuations in temperature and water availability may affect microbial niche space producing an environment conducive to the growth of opportunists. We detail the change in immune genes overwinter including pro-and antioxidant gene expression in the hypopharygeal gland, a secretory gland that interfaces with the extended social environment on many levels. We found major differences in the microbiome of stored pollen overwinter. The cold, controlled overwintering environment produced the healthiest result based on immune gene expression, and microbiome characteristics. Warm overwintering was associated changes in the midgut and mouthpart microbiota that suggest increased disease susceptibility, including significantly greater abundance of Enterobacteriaceae and Xanthomonadaceae in the worker midgut post-winter. Concurrently, the significant reduction in Xanthomonadaceae bacteria on the mouthparts of the same bees showing significantly greater abaecin gene expression in their hypopharengeal glands, and increased Xanthomonadaceae in their midguts suggests a hygienic response to hive microbiome opportunists. In general, we found many differences in microbiome structure between warm and cold overwintering environments. Our results may reflect selection pressures that shaped the social and hive microbiome with evolution to a perennial life history.