Routes of Acquisition of the Gut Microbiota of the Honey Bee Apis mellifera

Abstract

bStudies of newly emerged Apis mellifera worker bees have demonstrated that their guts are colonized by a consistent core microbiota within several days of eclosure. We conducted experiments aimed at illuminating the transmission routes and spatiotemporal colonization dynamics of this microbiota. Experimental groups of newly emerged workers were maintained in cup cages and exposed to different potential transmission sources. Colonization patterns were evaluated using quantitative real-time PCR (qPCR) to assess community sizes and using deep sequencing of 16S rRNA gene amplicons to assess community composition. In addition, we monitored the establishment of the ileum and rectum communities within workers sampled over time from natural hive conditions. The study verified that workers initially lack gut bacteria and gain large characteristic communities in the ileum and rectum within 4 to 6 days within hives. Typical communities, resembling those of workers within hives, were established in the presence of nurse workers or nurse worker fecal material, and atypical communities of noncore or highly skewed compositions were established when workers were exposed only to oral trophallaxis or hive components (comb, honey, bee bread). The core species of Gram-negative bacteria, Snodgrassella alvi, Gilliamella apicola, and Frischella perrara, were dependent on the presence of nurses or hindgut material, whereas some Gram-positive species were more often transferred through exposure to hive components. These results indicate aspects of the colony life cycle and behavior that are key to the propagation of the characteristic honey bee gut microbiota.

Transcriptional signatures of parasitization and markers of colony decline in Varroa-infested honey bees (Apis mellifera)

“…In our study, all the infested bees, from both the field and cage studies, showed a significant up-regulation of transcripts from the S. alvi genome in comparison with the uninfested ones (see data from Experiments 2 and 3 below). Previous studies investigating the composition of bee's core microbiota found that A. mellifera workers eclose without core resident bacteria and with a few bacteria of every kind (Gilliam, 1971;Martinson et al, 2012) and develop a stable microbial community by day 4e6 after exposure to the natural hive conditions (Powell et al, 2014;Anderson et al, 2015). This was certainly possible for bees from the field study but more difficult for those from the cage studies, since they were collected at the L5 stage and transferred to the lab until eclosion and sampled immediately after, in the case of newly emerged bees, or maintained in cages until sampling, in the case of adult bees.…”

Engineering Microbiomes to Improve Plant and Animal Health

“…Microbiome inheritance: perpetuation of a microbiome between hosts, typically between parent and offspring, but also between mates [80], siblings or other relatives (e.g., between members of a social-insect colony [61]…”

“…Vertical transmission can occur via a diversity of pathways, including transovarial transmission, or via behavioral mechanisms such as a mother coating an egg casing with bacteria which the offspring then acquires upon hatching [49,54]. Likewise, components of the human microbiome are inherited from a mother during or even before birth [53,60], and the honeybee gut microbiome of eight bacterial species[ 1 _ T D $ D I F F ] clusters is inherited by newborn bees from sibling workers or the hive environment [61,62]. Importantly, vertical transmission of microbiomes can occur with different degrees of fidelity, measured as the likelihood with which an individual microbial genotype or whole community is passed successfully from mother to offspring.…”

An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects

“…A central feature of many social and subsocial insects is the intimate interaction of conspecifics through behaviours such as trophallaxis, the transfer of food or other fluids through mouth-to-mouth (stomodeal) or anus-to-mouth ( proctodeal) feeding [27]. These behaviours can facilitate exchange of microbes among nest members, thereby contributing to maintenance of a beneficial microbiota, as has been demonstrated in ants [16,28,29], termites [30] and bees [31,32]. In fact, it has been speculated that the evolution of complex social forms could be reinforced, among other factors, by the convenience of acquiring beneficial microbes through recurring contact with conspecifics [33].…”

“…In honeybees (Apis mellifera), workers lack this distinctive microbial community upon eclosion, and recent findings demonstrate that they acquire the most dominant members of the microbiota either through social contact with nestmates (trophallaxis), specifically nurses, or via contact with the hive components (e.g. combs and honey) [32,36]. As for bumblebees, molecular analyses carried out across three host species (B. sonorus, B. impatientis and Bombus sp.)…”