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.
more »
« less
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
- Award ID(s):
- 1929499
- NSF-PAR ID:
- 10426741
- Date Published:
- Journal Name:
- Frontiers in Microbiology
- Volume:
- 13
- ISSN:
- 1664-302X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Introduction Interest for bee microbiota has recently been rising, alleviating the gap in knowledge in regard to drivers of solitary bee gut microbiota. However, no study has addressed the microbial acquisition routes of tropical solitary bees. For both social and solitary bees, the gut microbiota has several essential roles such as food processing and immune responses. While social bees such as honeybees maintain a constant gut microbiota by direct transmission from individuals of the same hive, solitary bees do not have direct contact between generations. They thus acquire their gut microbiota from the environment and/or the provision of their brood cell. To establish the role of life history in structuring the gut microbiota of solitary bees, we characterized the gut microbiota of Centris decolorata from a beach population in Mayagüez, Puerto Rico. Females provide the initial brood cell provision for the larvae, while males patrol the nest without any contact with it. We hypothesized that this behavior influences their gut microbiota, and that the origin of larval microbiota is from brood cell provisions. Methods We collected samples from adult females and males of C. decolorata ( n = 10 each, n = 20), larvae ( n = 4), and brood cell provisions ( n = 10). For comparison purposes, we also sampled co-occurring female foragers of social Apis mellifera ( n = 6). The samples were dissected, their DNA extracted, and gut microbiota sequenced using 16S rRNA genes. Pollen loads of A. mellifera and C. decolorata were analyzed and interactions between bee species and their plant resources were visualized using a pollination network. Results While we found the gut of A. mellifera contained the same phylotypes previously reported in the literature, we noted that the variability in the gut microbiota of solitary C. decolorata was significantly higher than that of social A. mellifera . Furthermore, the microbiota of adult C. decolorata mostly consisted of acetic acid bacteria whereas that of A. mellifera mostly had lactic acid bacteria. Among C. decolorata , we found significant differences in alpha and beta diversity between adults and their brood cell provisions (Shannon and Chao1 p < 0.05), due to the higher abundance of families such as Rhizobiaceae and Chitinophagaceae in the brood cells, and of Acetobacteraceae in adults. In addition, the pollination network analysis indicated that A. mellifera had a stronger interaction with Byrsonima sp. and a weaker interaction with Combretaceae while interactions between C. decolorata and its plant resources were constant with the null model. Conclusion Our data are consistent with the hypothesis that behavioral differences in brood provisioning between solitary and social bees is a factor leading to relatively high variation in the microbiota of the solitary bee.more » « less
-
null (Ed.)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.more » « less
-
null (Ed.)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.more » « less
-
Daniel, Sloan (Ed.)Abstract Recent declines in the health of the honey bee have startled researchers and lay people alike as honey bees are agriculture’s most important pollinator. Honey bees are important pollinators of many major crops and add billions of dollars annually to the US economy through their services. One factor that may influence colony health is the microbial community. Indeed, the honey bee worker digestive tract harbors a characteristic community of bee-specific microbes, and the composition of this community is known to impact honey bee health. However, the honey bee is a superorganism, a colony of eusocial insects with overlapping generations where nestmates cooperate, building a hive, gathering and storing food, and raising brood. In contrast to what is known regarding the honey bee worker gut microbiome, less is known of the microbes associated with developing brood, with food stores, and with the rest of the built hive environment. More recently, the microbe Bombella apis was identified as associated with nectar, with developing larvae, and with honey bee queens. This bacterium is related to flower-associated microbes such as Saccharibacter floricola and other species in the genus Saccharibacter, and initial phylogenetic analyses placed it as sister to these environmental bacteria. Here, we used comparative genomics of multiple honey bee-associated strains and the nectar-associated Saccharibacter to identify genomic changes that may be associated with the ecological transition to honey bee association. We identified several genomic differences in the honey bee-associated strains, including a complete CRISPR/Cas system. Many of the changes we note here are predicted to confer upon Bombella the ability to survive in royal jelly and defend themselves against mobile elements, including phages. Our results are a first step toward identifying potential function of this microbe in the honey bee superorganism.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fmicb.2022.1057626
