The honey bee "hive" microbiota: meta-analysis reveals a native and aerobic microbiota prevalent throughout the social resource niche

Authors: Anderson, Kirk; Copeland, Duan

Submitted to: Frontiers in Bee Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/19/2024
Publication Date: 7/5/2024
Citation: Anderson, K.E., Copeland, D.C. 2024. The honey bee "hive" microbiota: Meta-analysis reveals a native and aerobic microbiota prevalent throughout the social resource niche. Frontiers in Bee Science. 2. Article 1410331. https://doi.org/10.3389/frbee.2024.1410331.
DOI: https://doi.org/10.3389/frbee.2024.1410331

Interpretive Summary: Bacterial membership of the honey bee worker hindgut has been explored thoroughly revealing both composition and function. However, less effort has been devoted to the oxygen rich social niches associated with the nest environment and colony process. We performed a meta-analysis of 3800+ publicly available bar-code libraries examining the hypothesis of a social resource microbiota. We selected studies to represent tissue-specific samples, including various oxygen-rich environments throughout the colony and hive, defined by social process. These included queen and worker gut tissues, foregut, midgut, ileum, rectum, mouthparts, worker social glands, as well as secreted and stored nutrition and developing larvae. We found that the oxygen-rich foregut and midgut environments of queens and workers share a significant portion of their bacterial groups with that of larval rearing and nutrient storage, defining the social resource microbiota. Characterized by rapid growth, this shared social microbiota functions primarily in disease prevention at both the individual and colony level, but may also function in microbiome resilience under conditions that alter gut physiology. Defining the microbiota of social function contributes to a systems-based understanding of opportunistic disease, colony hygiene, and gut microbiome resilience in honey bees.

Technical Abstract: The microbiome of the honey bee worker hindgut has been explored thoroughly with culturing and next-generation sequencing revealing both composition and function. However, less effort has been devoted to the aerobic social niches associated with the hive environment and colony process. We performed a meta-analysis of 3,800+ publicly available 16S rRNA gene sequence libraries examining the hypothesis of a native aerobic microbiota associated with social interaction and colony resources. We selected high-throughput studies to represent tissue-specific samples, including nine distinct aerobic niches throughout the colony and hive, defined by social nutrient processing. These included queen and worker gut tissues, foregut, midgut, ileum, rectum, mouthparts, worker social glands, developing larvae, and secreted and stored nutrition. We found that the aerobic mouthparts, foregut and midgut niches of queens and workers share a significant portion of their microbiome with that of larval rearing and nutrient secretion and storage, defining the microbiota of the social resource niche. Characterized by species dominance and rapid growth, the social resource microbiota functions primarily in disease prevention at both the individual and colony level and may also function in social communication and gut microbiome resilience. Defining the microbiota of social function contributes to a systems-level understanding of host–microbial interactions in the honey bee.