Metal contaminant accumulation in the hive: Consequences for whole‐colony health and brood production in the honey bee (<i>Apis mellifera</i> L.)

Environmental Microbiology

Graystock

et al. 2019

Summary Bumble bees are important and widespread insect pollinators who face many environmental challenges. For example, bees are exposed to the metalloid selenate when foraging on pollen and nectar from plants growing in contaminated soils. As it has been shown that the microbiome of animals reduces metalloid toxicity, we assayed the ability of the bee microbiome to increase survivorship against selenate challenge. We exposed uninoculated or microbiota‐inoculated Bombus impatiens workers to a field‐realistic dose of 0.75 mg l−1 selenate and found that microbiota‐inoculated bees survive slightly but significantly longer than uninoculated bees. Using 16S rRNA gene sequencing, we found that selenate exposure altered gut microbial community composition and relative abundance of specific core bacteria. We also grew two core bumble bee microbes – Snodgrassella alvi and Lactobacillus bombicola – in selenate‐spiked media and found that these bacteria grew in the tested concentrations of 0.001–10 mg l−1 selenate. Furthermore, the genomes of these microbes harbour genes involved in selenate detoxification. The bumble bee microbiome slightly increases survivorship when the host is exposed to selenate, but the specific mechanisms and colony‐level benefits under natural settings require further study.

Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

The bumble bee microbiome increases survival of bees exposed to selenate toxicity

Environmental Microbiology

Graystock

et al. 2019

“…It is therefore worrisome that some populations of these important pollinators are declining in both Europe (3) and North America (4), with the main contributors of these declines thought to be habitat destruction, disease, and chemical exposure (5,6). While pesticides are considered to be the primary class of xenobiotics responsible for bee decline, foraging bees are exposed to additional environmental toxicants in floral nectar and pollen such as heavy metals (7), and oxidizers (8). The direct risks these chemicals pose to bees is not fully appreciated, furthermore, the indirect influences most chemicals (including pesticides) have on bee health is an understudied area (9,10).…”

Section: Introductionmentioning

confidence: 99%

“…Flowers produce oxidizers (16) and sequester heavy metals (17) to protect themselves from parasites and herbivores respectively. The hive products of honey bees foraging on flowers that are growing in soils contaminated with selenium ions, copper, and/or cadmium have been shown to accumulate these pollutants at concentrations greater than in the flowers (7). So frequent is this exposure and accumulation of contaminants that honey bees have been proposed as bioindicators of soil contamination whereby testing the hives’ honey for metals will indicate the presence of local environmental toxins (18).…”

Section: Introductionmentioning

confidence: 99%

The direct and indirect effects of environmental toxicants on the health of bumble bees and their microbiomes

Russell

et al. 2020

Preprint

Bumble bees (Bombus spp.) are important and widespread insect pollinators, but the act of foraging on flowers can expose them to harmful pesticides and environmental chemicals such as oxidizers and heavy metals. How these compounds directly influence bee survival and indirectly affect bee health via the gut microbiome is largely unknown. As the toxins and toxicants in floral nectar and pollen take many forms, we explored the genomes of core bumblebee microbes (Using RAST) for their potential to detoxify cadmium, copper, selenium, the neonicotinoid pesticide imidacloprid, and hydrogen peroxide - which have all been identified in floral nectar and pollen. We then exposed Bombus impatiens workers to varying concentrations of these chemicals spiked into their diet and identified the direct effects on bee survival. Using field realistic doses, we further explored indirect effects on bee microbiomes. We found multiple genes in core gut microbes that have the potential to aid in detoxifying harmful chemicals. We also found that while the chemicals are largely toxic at levels within and above field-realistic concentrations, the field-realistic concentrations - except for imidacloprid - altered the composition of the bee microbiome, potentially causing gut dysbiosis. Overall, our study shows that environmental chemicals found in floral nectar and pollen can directly cause bee mortality, and at field-realistic levels, likely have indirect, deleterious effects on bee health via their influence on the bee microbiome.

“…Along with other species, bee populations are declining around the world, most likely due to a combination of disease, pesticides, and land use change resulting in a lack of floral forage (4). Relatively unstudied stressors include the metals and metalloids that are harmful to bees and that can affect their overall health when bees forage on plants grown in contaminated areas (5,6). As bees may encounter various pollutants across environments (7), the capacity for diverse environmental stressors to affect bee health needs to be understood and mitigated.…”

mentioning

confidence: 99%

Cadmium and Selenate Exposure Affects the Honey Bee Microbiome and Metabolome, and Bee-Associated Bacteria Show Potential for Bioaccumulation

Kirkwood

et al. 2019

Appl Environ Microbiol

Honey bees are important insect pollinators used heavily in agriculture and can be found in diverse environments. Bees may encounter toxicants such as cadmium and selenate by foraging on plants growing in contaminated areas, which can result in negative health effects. Honey bees are known to have a simple and consistent microbiome that conveys many benefits to the host, and toxicant exposure may impact this symbiotic microbial community. We used 16S rRNA gene sequencing to assay the effects that sublethal cadmium and selenate treatments had over 7 days and found that both treatments significantly but subtly altered the composition of the bee microbiome. Next, we exposed bees to cadmium and selenate and then used untargeted liquid chromatography-mass spectrometry (LC-MS) metabolomics to show that chemical exposure changed the bees' metabolite profiles and that compounds which may be involved in detoxification, proteolysis, and lipolysis were more abundant in treatments. Finally, we exposed several strains of bee-associated bacteria in liquid culture and found that each strain removed cadmium from its medium but that only Lactobacillus Firm-5 microbes assimilated selenate, indicating the possibility that these microbes may reduce the metal and metalloid burden on their host. Overall, our report shows that metal and metalloid exposure can affect the honey bee microbiome and metabolome and that strains of bee-associated bacteria can bioaccumulate these toxicants. IMPORTANCE Bees are important insect pollinators that may encounter environmental pollution when foraging upon plants grown in contaminated areas. Despite the pervasiveness of pollution, little is known about the effects of these toxicants on honey bee metabolism and their symbiotic microbiomes. Here, we investigated the impact of selenate and cadmium exposure on the gut microbiome and metabolome of honey bees. We found that exposure to these chemicals subtly altered the overall composition of the bees' microbiome and metabolome and that exposure to toxicants may negatively impact both host and microbe. As the microbiome of animals can reduce mortality upon metal or metalloid challenge, we grew bee-associated bacteria in media spiked with selenate or cadmium. We show that some bacteria can remove these toxicants from their media in vitro and suggest that bacteria may reduce metal burden in their hosts.