Gut and Colony Microbiota of Honey Bees Apis mellifera: Social Immunity, Opportunistic Disease and Survival Overwinter.

Abstract

BackgroundOverwintering is a major contributor to honey bee colony loss and involves changes in environmental conditions, host physiology and group behavior that influence disease susceptibility. Honey bees possess a secretory head gland that interfaces with the extended colony environment on many levels, producing pro-oxidants, antioxidants and antimicrobial peptides. With the coming of winter, colonies produce a long-lived (diutinus) worker phenotype that survives until environmental conditions improve. We used a known-age worker cohort to investigate microbiome integrity and social gene expression of diutinus workers overwinter. We provide additional context by contrasting host-microbial interactions from warm outdoor and cold indoor overwintering environments. ResultsWe produce the first evidence that social immune gene expression is associated with the core hindgut and colony microbiota in honey bees, and highlight the midgut as a target of opportunistic disease overwinter. We discovered a distinct physiological and microbiological trajectory for diutinus workers that differs drastically from younger, short-lived workers in the colony. Diutinus bees were associated with decreased fungal load and decreased bacterial diversity, and increased core microbiota and longevity. Colonies overwintered indoors maintained a stable or improved microbiota structure and complimentary gene expression overwinter. In contrast, workers from colonies overwintered outdoors in warm southern conditions possessed changes co-occurring throughout the alimentary tract microbiota that suggest opportunistic disease progression and resistance in diutinus workers, but susceptibility to opportunistic disease in younger workers that emerged during the winter, including increases in Enterobacteriaceae, fungal load and bacterial diversity abundance. ConclusionsOur results highlight social selection pressures that shaped the colony and hindgut microbiome with evolution to a perennial life history. The results are consistent with a “group level” explanation of social immunity, including host associations with the colony microbiota, and a social immune response by long-lived diutinus workers to accompany microbial opportunism. The cost/benefit ratio associated with limited expression of the diutinus phenotype may be a strong determinant of colony survival overwinter. The relationship of colony and gut microbiota with social immune function highlights the range of host-microbial interaction associated with the honey bee superorganism, and its potential influence on colony health, disease resistance and gut integrity.