Development of the Honey Bee Gut Microbiome throughout the Queen-Rearing Process

Abstract

The European honey bee (Apis mellifera) is used extensively to produce hive products and for crop pollination, but pervasive concerns about colony health and population decline have sparked an interest in the microbial communities that are associated with these important insects. Currently, only the microbiome of workers has been characterized, while little to nothing is known about the bacterial communities that are associated with queens, even though their health and proper function are central to colony productivity. Here, we provide a large-scale analysis of the gut microbiome of honey bee queens during their developmental trajectory and through the multiple colonies that host them as part of modern queen-rearing practices. We found that queen microbiomes underwent a dramatic shift in size and composition as they aged and encountered different worker populations and colony environments. Queen microbiomes were dominated by enteric bacteria in early life but were comprised primarily of alphaproteobacteria at maturity. Furthermore, queen gut microbiomes did not reflect those of the workers who tended them and, indeed, they lacked many of the bacteria that are considered vital to workers. While worker gut microbiotas were consistent across the unrelated colony populations sampled, the microbiotas of the related queens were highly variable. Bacterial communities in mature queen guts were similar in size to those of mature workers and were characterized by dominant and specific alphaproteobacterial strains known to be associated with worker hypopharyngeal glands. Our results suggest a model in which queen guts are colonized by bacteria from workers' glands, in contrast to routes of maternal inoculation for other animal microbiomes.H oney bees (Apis spp.) are characterized by a highly partitioned reproductive division of labor, where a single queen lays the eggs that give rise to virtually all members of her colony, and her daughters, the workers, execute all other laborious jobs, including that of caring for her offspring (1). As the sole caregivers in the colony, workers share food extensively with one another, consuming their colony's food reserves and then distributing nutrients in various forms to their queen, other workers, and reproductive males (drones) (2). For all three of these castes, workers share food with adults through trophallaxis (mouth-to-mouth food transfer of liquids from one worker's gut to another's) or by feeding developing larvae brood food (glandular secretions derived from consumed nutrients). Because of these mechanisms of food distribution, a honey bee colony often is considered to have a "social stomach." Studies with tracers show rapid distribution (Ͻ24 h) of food from small numbers of individuals to many, if not the majority, of colony members across all ages and castes (3-7). Nurse-age bees (typically less than 10 days old) are the primary consumers of pollen (8); thus, they are the main distributors of pollen-based nutrients to adults and the brood that they rear (3, 5). Nectar als...

Interactions between Cooccurring Lactic Acid Bacteria in Honey Bee Hives

“…We found that honey bee larvae are colonized with Fructobacillus, Alpha-2.2, and Lactobacillales. Other studies of honey bee larvae also identified Alpha-2.2 and Lactobacilliales as early colonizers (24,44,45), suggesting that these clades may be commonly found with young, larval bees. It is important to note that these culture-based studies are dependent on the medium used to select for microbial members and that the medium used here (and in previous work) selects for acetic and lactic acid bacteria.…”

Honey bee gut microbial communities are robust to the fungicide Pristine® consumed in pollen

“…In the second experiment, we observed a large number of non-core bacteria, particularly P. apium , non-Firm 4 and Firm 5 Lactobacillus sp., Enterococcaceae , and the pathogen P. larvae . P. apium is found at lower levels in the gut (Corby-Harris et al 2014a;Martinson et al 2011;Martinson et al 2012;Moran et al 2012;Sabree et al 2012) and is typically more abundant in hive food stores (Anderson et al 2014), queens (Kapheim et al 2015;Tarpy et al 2015), larvae (Vojvodic et al 2013), and in the hypopharyngeal glands and crops of nurses (Corby-Harris et al 2014b). Because P. apium is relatively abundant in food stores, hypopharyngeal glands, and crop, one possibility is that the guts displaying high P. apium titers were recently inoculated through either pollen feeding or trophallaxis.…”

The role of the gut microbiome in health and disease of adult honey bee workers

“…Smaller numbers of bacteria, often representing environmental species, occur in the foregut and midgut [3]. The core species are relatively infrequent in larvae and in adult queens, which contain highly variable communities dominated by environmental bacteria [4, 5]. The mature worker hindgut microbiome is substantial, totaling 10 8 –10 9 bacterial cells [6] and is established in workers within four days following eclosure, before leaving the hive.…”

“…While a largely consistent microbiome persists throughout the lifespans of honey bee adult workers, adult queens have a strikingly different microbiome composition, with greater variation among individuals, and consisting of bacteria that are also found in the hive environment [4 • ,5]. The size of the queen microbiome is highly variable but often smaller than that of workers.…”