Honey bees as models for gut microbiota research

Abstract

The gut microbiota of the honey bee (Apis mellifera) offers several advantages as an experimental system for addressing how gut communities affect their hosts and for exploring the processes that determine gut community composition and dynamics. A small number of bacterial species dominate the honey bee gut community. These species are restricted to bee guts and can be grown axenically and genetically manipulated. Large numbers of microbiota-free hosts can be economically reared and then inoculated with single isolates or defined communities to examine colonization patterns and effects on host phenotypes. Honey bees have been studied extensively, due to their importance as agricultural pollinators and as models for sociality. Because of this history of bee research, the physiology, development, and behavior of honey bees is relatively well understood, and established behavioral and phenotypic assays are available. To date, studies on the honey bee gut microbiota show that it affects host nutrition, weight gain, endocrine signaling, immune function, and pathogen resistance, while perturbation of the microbiota can lead to reduced host fitness. As in humans, the microbiota is concentrated in the distal part of the gut, where it contributes to digestion and fermentation of plant cell wall components. Much like the human gut microbiota, many bee gut bacteria are specific to the bee gut and can be directly transmitted between individuals through social interaction. Although simpler than the human gut microbiota, the bee gut community presents opportunities to understand the processes that govern the assembly of specialized gut communities as well as the routes through which gut communities impact host biology.

Figure 1.

Similarities (center) and differences (right and left sides) between the gut microbiota of humans and the gut microbiota of honey bees. SCFA, short chain fatty acids.

Figure 2.

Design of gnotobiotic honey bee studies. Microbiota-free (MF) hosts emerge in the lab (a) where they can be inoculated with isolated gut symbiont strains, genetically modified symbionts, or natural communities (b). These bees may be maintained in laboratory conditions or marked and returned to the hive environment (c). Destructive sampling of bees and sequencing allows for analyses of community composition and function. Alternatively, phenotypic (e.g., behavioral) assays, can reveal effects of defined gut communities on bees, while genetically modified (GM) fluorescent strains facilitate in situ imaging of bacteria (d).

Figure 3.

Summary of the effects of the honey bee gut microbiota on host and the gut microbial metabolism. The dominant members in the ileum and rectum ferment sugars and polysaccharides from the host diet (honey and pollen) to SCFAs. Oxygen consumption by the species S. alvi, which forms a layer attached to the inner gut wall, maintains an anoxic gut environment. The presence of gut bacteria can also reduce the gut pH and redox potential. Moreover, gut bacteria have various effects on the weight gains, insulin signaling, behaviors, and pathogen resistance of the hosts.