Different insect groups are host to a broad diversity of gut microbial communities, which vary in complexity, extent of adaptation to the host gut environment,

A distinctive microbial community of approximately nine bacterial species clusters inhabits the bee gut. These bacteria are host-adapted, and each species cluster occupies particular niches and spatial locations in the bee. The gut microbial community of the bee is transmitted through social contact, similar to the mode of transmission in mammals. The characteristic microbial community of the bee gut can be perturbed and invaded by opportunistic microorganisms, which resembles disease states in humans. There is substantial strain-level diversity in the bee gut microbiota, with individual strains harbouring unique sets of genes with distinct functional capabilities. How this diversity arises and is maintained is not well understood. Metabolically, most members of the microbial community in the bee gut are fermentative, breaking down the carbohydrate-rich diet of bees into products, such as lactic acid and acetate. Although not yet well-established, these fermentative microorganisms may have a role in contributing to the nutrition of hosts. The normal bee gut microbiota has been associated with lower levels of infection with pathogens, which may indicate a beneficial role of the microbiota for the host bee. The bee gut microbiota can be cultured in vitro, and gnotobiotic bees can be easily produced, which makes bees a tractable model for the study of the symbiosis of gut microorganisms.

Glyphosate, the primary herbicide used globally for weed control, targets the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) enzyme in the shikimate pathway found in plants and some microorganisms. Thus, glyphosate may affect bacterial symbionts of animals living near agricultural sites, including pollinators such as bees. The honey bee gut microbiota is dominated by eight bacterial species that promote weight gain and reduce pathogen susceptibility. The gene encoding EPSPS is present in almost all sequenced genomes of bee gut bacteria, indicating that they are potentially susceptible to glyphosate. We demonstrated that the relative and absolute abundances of dominant gut microbiota species are decreased in bees exposed to glyphosate at concentrations documented in the environment. Glyphosate exposure of young workers increased mortality of bees subsequently exposed to the opportunistic pathogen Serratia marcescens. Members of the bee gut microbiota varied in susceptibility to glyphosate, largely corresponding to whether they possessed an EPSPS of class I (sensitive to glyphosate) or class II (insensitive to glyphosate). This basis for differences in sensitivity was confirmed using in vitro experiments in which the EPSPS gene from bee gut bacteria was cloned into Escherichia coli. All strains of the core bee gut species, Snodgrassella alvi, encode a sensitive class I EPSPS, and reduction in S. alvi levels was a consistent experimental result. However, some S. alvi strains appear to possess an alternative mechanism of glyphosate resistance. Thus, exposure of bees to glyphosate can perturb their beneficial gut microbiota, potentially affecting bee health and their effectiveness as pollinators. Significance Increased mortality of honey bee colonies has been attributed to several factors but is not fully understood. The herbicide glyphosate is expected to be innocuous to animals, including bees, because it targets an enzyme only found in plants and microorganisms. However, bees rely on a specialized gut microbiota that benefits growth and provides defense against pathogens. Most bee gut bacteria contain the enzyme targeted by glyphosate, but vary in whether they possess susceptible versions and, correspondingly, in tolerance to glyphosate. Exposing bees to glyphosate alters the bee gut community and increases susceptibility to infection by opportunistic pathogens. Understanding how glyphosate impacts bee gut symbionts and bee health will help elucidate a possible role of this chemical in colony decline.

Significance: Honey bees are globally important plant pollinators. Guts of adult workers contain specialized bacteria not found outside bees. Experimental results show that gut bacteria increase weight gain in young adult bees, affect expression of genes governing insulin and vitellogenin levels, and increase sucrose sensitivity. Gut bacteria also shape the physicochemical conditions within the gut, lowering pH and oxygen levels. Peripheral resident bacteria consume oxygen, thus maintaining anoxia, as required for microbial activity. Additionally, gut bacteria produce short-chain fatty acids, with acetate and propionate as the major metabolites, as in guts of human and other animals. This study demonstrates how bacteria in the honey bee gut affect host weight gain and improves our understanding of how gut symbionts influence host health.

Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sap-feeding insects, and Buchnera aphidicola , a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host–symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host–pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphid– Buchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.

Honey bees, bumble bees, and stingless bees have related gut microbial communities that are shaped by host evolutionary history.