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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.
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Environmentally acquired gut-associated bacteria are not critical for growth and survival in a solitary bee, Megachile rotundata
ABSTRACT 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.IMPORTANCEThis 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.
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- PAR ID:
- 10544088
- Editor(s):
- Tortosa, Pablo
- Publisher / Repository:
- American Society of Microbiology
- Date Published:
- Journal Name:
- Applied and Environmental Microbiology
- Volume:
- 90
- Issue:
- 9
- ISSN:
- 0099-2240
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The microbial composition of stored food can influence its stability and determine the microbial species consumed by the organism feeding on it. Many bee species store nectar and pollen in provisions constructed to feed developing offspring. Previous work has shown variation in provision microbiome among bee populations, yet whether this variation is determined by the pollen types within provisions, variation between bee species at the same nesting sites, or geographic distance was unclear. Here, we sampled two species of co-occurring cavity nesting bees in the genusOsmiaat 13 sites across the Sierra foothills in California and examined the composition of pollen, fungi and bacteria found in their provisions across sites. As expected, pollen, bacterial and fungal composition exhibited significant turnover between bees and sites, with bee species characterized by particular pollen and microbial species. Pollen composition explained 15% of variation in bacterial composition and ∼30% of variation in fungal composition, whereas spatial distance among sites explained minimal additional variation. Symbiotic or bee-specialized microbe generaAscosphaera,SodalisandWolbachiashowed contrasting patterns of association with pollen composition, suggesting distinct acquisition and transmission routes for each. Comparing provisions from both bee species comprised of the same pollens points to environmental acquisition rather than bee species as a key factor shaping the early stages of the bee microbiome inOsmia. The patterns we observed also contrast withApilactobacillus-dominated provision microbiome in other solitary bee species, suggesting variable mechanisms of microbial assembly in stored food among bee species.more » « less
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Abstract The microbial composition of stored food can influence its stability and the microbial species consumed by the organism feeding on it. Many bee species store nectar and pollen in provisions constructed to feed developing offspring. Yet, whether microbial composition is determined by the pollen types within provisions, variation between bee species at the same nesting sites, or geographic distance was unclear. Here, we sampled two species of cooccurring cavity nesting bees in the genus Osmia at 13 sites in California and examined the composition of pollen, fungi, and bacteria in provisions. Pollen composition explained 15% of variation in bacterial composition and ∼30% of variation in fungal composition, whereas spatial distance among sites explained minimal additional variation. Symbiotic microbe genera Ascosphaera, Sodalis, and Wolbachia showed contrasting patterns of association with pollen composition, suggesting distinct acquisition and transmission routes for each. Comparing provisions from both bee species comprised of the same pollens points to environmental acquisition rather than bee species as a key factor shaping the early stages of the bee microbiome in Osmia. The patterns we observed also contrast with Apilactobacillus-dominated provision microbiome in other solitary bee species, suggesting variable mechanisms of microbial assembly in stored food among bee species.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/aem.02076-23
