Gut microbiota structure differs between honey bees in winter and summer

Abstract

24Adult honey bees harbor a specialized gut microbiota of relatively low complexity. While 25 seasonal differences in community composition have been reported, previous studies have 26 focused on compositional changes rather than differences in absolute bacterial loads. 27 Moreover, little is known about the gut microbiota of winter bees, which live much longer 28 than bees during the foraging season, and which are critical for colony survival. We 29 quantified seven core members of the bee gut microbiota in a single colony over two years 30 and characterized the community composition in 14 colonies during summer and winter. 31Our data shows that total bacterial loads substantially differ between foragers, nurses, and 32 winter bees. Long-lived winter bees had the highest bacterial loads and the lowest 33 community α-diversity, with a characteristic shift towards high levels of Bartonella and 34 Commensalibacter, and a reduction of opportunistic colonizers. Using gnotobiotic bee 35 experiments, we show that diet is a major contributor to the observed differences in 36 bacterial loads. Overall, our study reveals that the gut microbiota of winter bees is 37 remarkably different from foragers and nurses. Considering the importance of winter bees 38 for colony survival, future work should focus on the role of the gut microbiota in winter 39 bee health and disease. 40 41 . CC-BY-NC-ND 4.0 International license author/funder. It is made available under a The copyright holder for this preprint (which was not peer-reviewed) is the . https://doi.org/10.1101/703512 doi: bioRxiv preprint 42 The European honey bee, Apis mellifera, is an important pollinator species for natural 43 ecosystems and agricultural production [1]. Its health status is threatened by numerous 44 factors including habitat loss, pesticide exposure, and high parasite and pathogen loads [2-45 4]. Accumulating evidence suggests that the gut microbiota of adult honey bees plays a 46 critical role for bee health [5]. The bee microbiota converts dietary compounds [6, 7] and 47 produces short chain fatty acids [8] in the gut, enhances sucrose responsiveness of the host 48 [8], and stimulates the immune system [9, 10]. Moreover, disruption of the gut microbiota 49 composition by antibiotic treatment, pesticide exposure, or dietary manipulations has 50 been associated with increased pathogen loads resulting in increased host mortality [11-51 14]. 52 A striking feature of the honey bee gut microbiota is its low taxonomic complexity. In 53 worker bees, the community is dominated by less than ten phylotypes (i.e. clusters of 54 strains sharing ≥97% sequence identity in the 16S rRNA gene), which typically make up 55 >95% of the bacterial cells in the gut [5, 15-18]. These phylotypes have been consistently 56 detected in honey bees, regardless of geographic location, life stage, or season [16, 19, 20], 57 and are acquired horizontally through contact with nest mates and hive components [21]. 58 They include five core phylotypes (Gilliamella, Snodgrassella, Lactoba...

Bee foraging preferences, microbiota and pathogens revealed by direct shotgun metagenomics of honey

“…Frischella perrara was more abundantly detected in spring, which is in accordance with the findings of previous studies (Kešnerová et al, 2020). Functional annotation of the autumn-specific bacteria identified functions related to carbohydrate metabolism, amino acid process and transport, and transposition.…”

“…), and the presence of additional noncore members ( Frischella perrara , Bartonella apis ) (Engel et al, 2012; Jones et al, 2018). Interestingly, recent studies also revealed individual‐specific microbiomes, reflecting potential roles in adaptive functions, such as fluctuation of metabolic potential and nutritive resources across seasons, as well as social status (Ellegaard & Engel, 2019; Kešnerová et al, 2020; Yun et al, 2018). Honeybee pathogens, such as Varroa destructor , brood diseases and Nosema ceranae , are detected mainly by hive inspection and conventional PCR, which often leads to delayed treatment initiation (López‐Uribe et al, 2020; Samuelson et al, 2020).…”

Acetobacteraceae in the honey bee gut comprise two distant clades with diverging metabolism and ecological niches

“…Alpha2.1 persisted in the gut environment and even significantly increased relative 627 to foragers and nurses sampled in summer (Kešnerová, et al 2019). The same pattern 628 was also observed for another community member of the bee gut microbiota, 629…”

Amplicon sequencing of variable 16S rRNA and ITS2 regions reveal honeybee susceptibility to diseases resulted of their dietary preferences under anthropogenic landforms

“…Adult honeybees harbour specialized gut microbiota of relatively low complexity with five core bacterial strains [3,4,24,25,26]: Lactobacillus Firm-4 and Firm-5 (Firmicutes), Giliamella (γ-proteobacteria, Orbales), Snodgrassella (γ-proteobacteria, Neisseriaceae), Bifidobacterium (Actinobacteria) and a number of elective bacterial strains, including Frischella (γ-proteobacteria, Orbales), Bartonella (α-proteobacteria, Rhizobiales), Commensalibacter (α-proteobacteria, Acetobacterales) and Bombella (α-proteobacteria, Acetobacterales), which was also confirmed in this study (Figure 1, Figure 2 1, Table 1, Table 2).…”

“…The next-generation sequencing (NGS) is a culture-independent method often used for studding entire microbial communities and helps to understand how microbes influence health and diseases of humans and animals including a honeybee [1][2][3]. Adult honeybees harbor a specialized gut microbiota of relatively low complexity with diet as a major factor to differences in bacterial loads [4]. Although honeybee microbiome core species is quite consistent regardless of environmental, geographical and genetic differences between specimens [2], some studies indicated that it can be sensitive to infections, changes in diet, malnutrition and many anthropogenic activities, as extensive pesticide use and urban land-use changes [5][6][7].…”