Beehives possess their own distinct microbiomes

Abstract

Background: Honeybees use plant material to manufacture their own food. These insect pollinators visit flowers repeatedly to collect nectar and pollen, which are shared with other hive bees to produce honey and beebread. While producing these products, beehives accumulate a considerable number of microbes, including bacteria that derive from plants and different parts of the honeybees' body. Whether bacteria form similar communities amongst beehives, even if located in close proximity, is an ecologically important question that has been addressed in this study. Specific ecological factors such as the surrounding environment and the beekeeping methods used can shape the microbiome of the beehive as a whole, and eventually influence the health of the honeybees and their ecosystem.

Results: We conducted 16S rRNA meta-taxonomic analysis on honey and beebread samples that were collected from 15 apiaries in the southeast of England to quantify the bacteria associated with different beehives. We observed that honeybee products carry a significant variety of bacterial groups that comprise bee commensals, environmental bacteria and symbionts and pathogens of plants and animals. Remarkably, this bacterial diversity differs not only amongst apiaries, but also between the beehives of the same apiary. In particular, the levels of the bee commensals varied significantly, and their fluctuations correlated with the presence of different environmental bacteria and various apiculture practices.

Conclusions: Our results show that every hive possesses their own distinct microbiome and that this very defined fingerprint is affected by multiple factors such as the nectar and pollen gathered from local plants, the management of the apiaries and the bacterial communities living around the beehives. Based on our findings, we suggest that the microbiome of beehives could be used as a valuable biosensor informing of the health of the honeybees and their surrounding environment.

Keywords: Apiary; Beehives; Gut commensals; Honey; Honeybees; Microbiome; Pollen.

Fig. 1

The observed-OTUs richness and inverse Simpson index of bacterial communities found in beehives and grouped by the type of sample (A) and different apiaries (B). Tukey–Kramer post-hoc analysis was carried out for multiple comparisons (*, p < 0.05)

Fig. 2

PCoA plots of the Jaccard (A) and Bray–Curtis (B) dissimilarities for bacterial communities (OTUs) found in samples of honey and pollen that were collected from the 15 different apiaries selected in this study. Samples with the same colour derive from the same apiary

Fig. 3

Bacterial communities of bee symbionts (orange), invertebrate symbionts (pink), vertebrate symbionts (yellow), environmental bacteria (green), and pathogens (red) found in honey (A) and pollen (B) samples. Other bacteria from which only the genus was identified are indicated in blue, while those unclassified are represented in grey. The species-level analysis of the identified OTUs revealed: (i) Bee symbionts (orange) isolated from honey, pollen and honeybees, including Arsenophonus nasoniae, Bartonella apis, Bombilactobacillus mellis, Frischella perrara, Gilliamella apicola, Lactobacillus kunkeei, L. helsingborgensis, L. apis, Parasaccharibacter apium, Snodgrassella alvi, and Spiroplasma melliferum; (ii) Invertebrate symbionts (pink) found in other insects and nematods, including Commensalibacter intestine, Moraxella osloensis, Photorhabdus kayaii and Serratia symbiotica; (iii) Vertebrate symbionts (yellow) found in the skin and gut of birds, mammals and humans, including Acinetobacter pullicarnis, Haemophilus parainfluenzae, Lactobacillus salivarius, and Microbacterium hominis; (iv) Environmental bacteria (green) found in water, soil, plants, seeds, fruits, food and animal faeces, some of which may cause infections in plants and animals, such as Acinetobacter boissieri, A. chinensis, A. junii, Bacillus thuringiensis, Brevundimonas diminuta, B. mediterranea, Burkholderia cepacia, Cutibacterium acnes, Fructobacillus fructosus, F. tropaeoli, Lactococcus lactis, Leuconostoc mesenteroides, Methyloversatilis discipulorum, Neokomagataea tanensis, Pantoea vagans, P. agglomerans, Pelomonas puraquae, Pseudomonas fluorescens, P. graminis, and Zymobacter palmae; (v) Pathogens (red) that cause diseases in plants, animals and humans, including Enterococcus faecalis, Lonsdalea britannica, Pseudomonas syringae, Staphylococcus aureus, Xanthomonas campestris, and Yersinia mollaretii; and (vi) other bacteria (blue) representing vertebrate symbionts and environmental bacteria, including Acinetobacter, Erwinia, Fibrobacter, Mycoplasma, Pantoea, Prevotella, Ralstonia, and Undibacterium