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Title: Solitary bee larvae modify bacterial diversity of pollen provisions in the stem-nesting bee, Osmia cornifrons (Megachilidae)
Microbes, including diverse bacteria and fungi, play an important role in the health of both solitary and social bees. Among solitary bee species, in which larvae remain in a closed brood cell throughout development, experiments that modified or eliminated the brood cell microbiome through sterilization indicated that microbes contribute substantially to larval nutrition and are in some cases essential for larval development. To better understand how feeding larvae impact the microbial community of their pollen/nectar provisions, we examine the temporal shift in the bacterial community in the presence and absence of actively feeding larvae of the solitary, stem-nesting bee, Osmia cornifrons (Megachilidae). Our results indicate that the O . cornifrons brood cell bacterial community is initially diverse. However, larval solitary bees modify the microbial community of their pollen/nectar provisions over time by suppressing or eliminating rare taxa while favoring bacterial endosymbionts of insects and diverse plant pathogens, perhaps through improved conditions or competitive release. We suspect that the proliferation of opportunistic plant pathogens may improve nutrient availability of developing larvae through degradation of pollen. Thus, the health and development of solitary bees may be interconnected with pollen bacterial diversity and perhaps with the propagation of plant pathogens. more »« less
Social bees have been extensively studied for their gut microbial functions, but the significance of the gut microbiota in solitary bees remains less explored. Solitary bee,Megachile rotundatafemales provision their offspring with pollen from various plant species, harboring a diverse microbial community that colonizes larvae guts. TheApilactobacillusis the most abundant microbe, but evidence concerning the effects ofApilactobacillusand other provision microbes on growth and survival are lacking. We hypothesized that the presence ofApilactobacillusin abundance would enhance larval and prepupal development, weight, and survival, while the absence of intact microbial communities was expected to have a negative impact on bee fitness. We reared larvae on pollen provisions with naturally collected microbial communities (Natural pollen) or devoid of microbial communities (Sterile pollen). We also assessed the impact of introducingApilactobacillus micheneriby adding it to both types of pollen provisions. Feeding larvae with sterile pollen +A. micheneriled to the highest mortality rate, followed by natural pollen +A. micheneri, and sterile pollen. Larval development was significantly delayed in groups fed with sterile pollen. Interestingly, larval and prepupal weights did not significantly differ across treatments compared to natural pollen-fed larvae. 16S rRNA gene sequencing found a dominance ofSodalis, whenA. micheneriwas introduced to natural pollen. The presence ofSodaliswith abundantA. micheneri suggests potential crosstalk between both, shaping bee nutrition and health. Hence, this study highlights that the reliance on nonhost-specific environmental bacteria may not impact fitness ofM. rotundata.
IMPORTANCE
This study investigates the impact of environmentally acquired gut microbes of solitary bee fitness with insights into the microbial ecology of bee and their health. While the symbiotic microbiome is well-studied in social bees, the role of environmental acquired microbiota in solitary bees remains unclear. Assessing this relationship in a solitary pollinator, the leaf-cutting bee,Megachile rotundata, we discovered that this bee species does not depend on the diverse environmental bacteria found in pollen for either its larval growth or survival. Surprisingly, high concentrations of the most abundant pollen bacteria, Apilactobacillus micheneridid not consistently benefit bee fitness, but caused larval mortality. Our findings also suggest an interaction betweenApilactobacillusand theSodalisand perhaps their role in bee nutrition. Hence, this study provides significant insights that contribute to understanding the fitness, conservation, and pollination ecology of other solitary bee species in the future.
Pathogens and parasites of solitary bees have been studied for decades, but the microbiome as a whole is poorly understood for most taxa. Comparative analyses of microbiome features such as composition, abundance, and specificity, can shed light on bee ecology and the evolution of host–microbe interactions. Here we study microbiomes of ground-nesting cellophane bees (Colletidae: Diphaglossinae). From a microbial point of view, the diphaglossine genus Ptiloglossa is particularly remarkable: their larval provisions are liquid and smell consistently of fermentation. We sampled larval provisions and various life stages from wild nests of Ptiloglossa arizonensis and two species of closely related genera: Caupolicana yarrowi and Crawfordapis luctuosa . We also sampled nectar collected by P. arizonensis . Using 16S rRNA gene sequencing, we find that larval provisions of all three bee species are near-monocultures of lactobacilli. Nectar communities are more diverse, suggesting ecological filtering. Shotgun metagenomic and phylogenetic data indicate that Ptiloglossa culture multiple species and strains of Apilactobacillus , which circulate among bees and flowers. Larval lactobacilli disappear before pupation, and hence are likely not vertically transmitted, but rather reacquired from flowers as adults. Thus, brood cell microbiomes are qualitatively similar between diphaglossine bees and other solitary bees: lactobacilli-dominated, environmentally acquired, and non-species-specific. However, shotgun metagenomes provide evidence of a shift in bacterial abundance. As compared with several other bee species, Ptiloglossa have much higher ratios of bacterial to plant biomass in larval provisions, matching the unusually fermentative smell of their brood cells. Overall, Ptiloglossa illustrate a path by which hosts can evolve quantitatively novel symbioses: not by acquiring or domesticating novel symbionts, but by altering the microenvironment to favor growth of already widespread and generalist microbes.
Climate change is rapidly warming thermal environments, an important abiotic stimulus governing interactions between microbial symbionts and their hosts. Increasing evidence suggests that solitary bees rely on pollen provision microbes for successful development. However, the effects of heat stress on provision microbiota and the resulting consequences for larval health and development remain to be examined. We performed an in vitro study to investigate the effects of the thermal environment on provision microbiome composition and measured fitness outcomes forOsmia lignarialarvae. While pollen sterilisation removed bacteria from microbe‐rich provisions, larval survivorship did not significantly differ between bees reared on microbe‐rich (unmanipulated) diets and provisions treated with ethylene oxide (EO) gas. In contrast to previous research in solitary bees, larvae reared on EO‐treated provisions weighed more and had higher total fat content, with temperature moderating the degree of difference. As anticipated, we observed a negative relationship between the duration of larval development and temperature. Our results indicated that an intact provision microbiota may not always improve bee fitness and that bee‐microbe interactions during larval development may contribute to the size‐shrinking effect observed for cavity‐nesting bees under warming conditions.
Bees collect pollen from flowers for their offspring, and by doing so contribute critical pollination services for our crops and ecosystems. Unlike many managed bee species, wild bees are thought to obtain much of their microbiome from the environment. However, we know surprisingly little about what plant species bees visit and the microbes associated with the collected pollen. Here, we addressed the hypothesis that the pollen and microbial components of bee diets would change across the range of the bee, by amplicon sequencing pollen provisions of a widespread small carpenter bee, Ceratina calcarata, across three populations. Ceratina calcarata was found to use a diversity of floral resources across its range, but the bacterial genera associated with pollen provisions were very consistent. Acinetobacter, Erwinia, Lactobacillus, Sodalis, Sphingomonas and Wolbachia were among the top ten bacterial genera across all sites. Ceratina calcarata uses both raspberry (Rubus) and sumac (Rhus) stems as nesting substrates, however nests within these plants showed no preference for host plant pollen. Significant correlations in plant and bacterial co-occurrence differed between sites, indicating that many of the most common bacterial genera have either regional or transitory floral associations. This range-wide study suggests microbes present in brood provisions are conserved within a bee species, rather than mediated by climate or pollen composition. Moving forward, this has important implications for how these core bacteria affect larval health and whether these functions vary across space and diet. These data increase our understanding of how pollinators interact with and adjust to their changing environment.
Mounting evidence suggests that microbes found in the pollen provisions of wild and solitary bees are important drivers of larval development. As these microbes are also known to be transmitted via the environment, most likely from flowers, the diet breadth of a bee may affect the diversity and identity of the microbes that occur in its pollen provisions. Here, we tested the hypothesis that, due to the importance of floral transmission of microbes, diet breadth affects pollen provision microbial community composition. We collected pollen provisions at four sites from the polylectic bee Osmia lignaria and the oligolectic bee Osmia ribifloris. We used high-throughput sequencing of the bacterial 16S rRNA gene to characterize the bacteria found in these provisions. We found minimal overlap in the specific bacterial variants in pollen provisions across the host species, even when the bees were constrained to foraging from the same flowers in cages at one site. Similarly, there was minimal overlap in the specific bacterial variants across sites, even within the same host species. Together, these findings highlight the importance of environmental transmission and host specific sorting influenced by diet breadth for microbes found in pollen provisions. Future studies addressing the functional consequences of this filtering, along with tests for differences between more species of oligoletic and polylectic bees will provide rich insights into the microbial ecology of solitary bees.
Kueneman, Jordan G., Gillung, Jessica, Van Dyke, Maria T., Fordyce, Rachel F., and Danforth, Bryan N. Solitary bee larvae modify bacterial diversity of pollen provisions in the stem-nesting bee, Osmia cornifrons (Megachilidae). Retrieved from https://par.nsf.gov/biblio/10426741. Frontiers in Microbiology 13. Web. doi:10.3389/fmicb.2022.1057626.
Kueneman, Jordan G., Gillung, Jessica, Van Dyke, Maria T., Fordyce, Rachel F., & Danforth, Bryan N. Solitary bee larvae modify bacterial diversity of pollen provisions in the stem-nesting bee, Osmia cornifrons (Megachilidae). Frontiers in Microbiology, 13 (). Retrieved from https://par.nsf.gov/biblio/10426741. https://doi.org/10.3389/fmicb.2022.1057626
Kueneman, Jordan G., Gillung, Jessica, Van Dyke, Maria T., Fordyce, Rachel F., and Danforth, Bryan N.
"Solitary bee larvae modify bacterial diversity of pollen provisions in the stem-nesting bee, Osmia cornifrons (Megachilidae)". Frontiers in Microbiology 13 (). Country unknown/Code not available. https://doi.org/10.3389/fmicb.2022.1057626.https://par.nsf.gov/biblio/10426741.
@article{osti_10426741,
place = {Country unknown/Code not available},
title = {Solitary bee larvae modify bacterial diversity of pollen provisions in the stem-nesting bee, Osmia cornifrons (Megachilidae)},
url = {https://par.nsf.gov/biblio/10426741},
DOI = {10.3389/fmicb.2022.1057626},
abstractNote = {Microbes, including diverse bacteria and fungi, play an important role in the health of both solitary and social bees. Among solitary bee species, in which larvae remain in a closed brood cell throughout development, experiments that modified or eliminated the brood cell microbiome through sterilization indicated that microbes contribute substantially to larval nutrition and are in some cases essential for larval development. To better understand how feeding larvae impact the microbial community of their pollen/nectar provisions, we examine the temporal shift in the bacterial community in the presence and absence of actively feeding larvae of the solitary, stem-nesting bee, Osmia cornifrons (Megachilidae). Our results indicate that the O . cornifrons brood cell bacterial community is initially diverse. However, larval solitary bees modify the microbial community of their pollen/nectar provisions over time by suppressing or eliminating rare taxa while favoring bacterial endosymbionts of insects and diverse plant pathogens, perhaps through improved conditions or competitive release. We suspect that the proliferation of opportunistic plant pathogens may improve nutrient availability of developing larvae through degradation of pollen. Thus, the health and development of solitary bees may be interconnected with pollen bacterial diversity and perhaps with the propagation of plant pathogens.},
journal = {Frontiers in Microbiology},
volume = {13},
author = {Kueneman, Jordan G. and Gillung, Jessica and Van Dyke, Maria T. and Fordyce, Rachel F. and Danforth, Bryan N.},
}
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