Adult honeybees harbor a specialized gut microbiota of relatively low complexity. While seasonal differences in community composition have been reported, previous studies have focused on compositional changes rather than differences in absolute bacterial loads. Moreover, little is known about the gut microbiota of winter bees, which live much longer than bees during the foraging season, and which are critical for colony survival. We quantified seven core members of the bee gut microbiota in a single colony over 2 years and characterized the community composition in 14 colonies during summer and winter. Our data show that total bacterial loads substantially differ between foragers, nurses, and winter bees. Long-lived winter bees had the highest bacterial loads and the lowest community α-diversity, with a characteristic shift toward high levels of Bartonella and Commensalibacter, and a reduction of opportunistic colonizers. Using gnotobiotic bee experiments, we show that diet is a major contributor to the observed differences in bacterial loads. Overall, our study reveals that the gut microbiota of winter bees is remarkably different from foragers and nurses. Considering the importance of winter bees for colony survival, future work should focus on the role of the gut microbiota in winter bee health and disease.
As pollinators, bees are cornerstones for terrestrial ecosystem stability and key components in agricultural productivity. All animals, including bees, are associated with a diverse community of microbes, commonly referred to as the microbiome. The bee microbiome is likely to be a crucial factor affecting host health. However, with the exception of a few pathogens, the impacts of most members of the bee microbiome on host health are poorly understood. Further, the evolutionary and ecological forces that shape and change the microbiome are unclear. Here, we discuss recent progress in our understanding of the bee microbiome, and we present challenges associated with its investigation. We conclude that global coordination of research efforts is needed to fully understand the complex and highly dynamic nature of the interplay between the bee microbiome, its host, and the environment. High-throughput sequencing technologies are ideal for exploring complex biological systems, including host-microbe interactions. To maximize their value and to improve assessment of the factors affecting bee health, sequence data should be archived, curated, and analyzed in ways that promote the synthesis of different studies. To this end, the BeeBiome consortium aims to develop an online database which would provide reference sequences, archive metadata, and host analytical resources. The goal would be to support applied and fundamental research on bees and their associated microbes and to provide a collaborative framework for sharing primary data from different research programs, thus furthering our understanding of the bee microbiome and its impact on pollinator health.
Gut bacteria engage in various symbiotic interactions with their host and impact gut immunity and homeostasis in different ways. In honey bees, the gut microbiota is composed of a relatively simple, but highly specialized bacterial community. One of its members, the gammaproteobacterium Frischella perrara induces the so-called scab phenotype, a dark-coloured band that develops on the epithelial surface of the pylorus. To understand the underlying host response, we analysed transcriptome changes in the pylorus in response to bacterial colonization. We find that, in contrast to the gut bacterium Snodgrassella alvi, F. perrara causes strong activation of the host immune system. Besides pattern recognition receptors, antimicrobial peptides and transporter genes, the melanization cascade was upregulated by F. perrara, suggesting that the scab phenotype corresponds to a melanization response of the host. In addition, transcriptome analysis of hive bees with and without the scab phenotype showed that F. perrara also stimulates the immune system under in-hive conditions in the presence of other gut bacterial species. Collectively, our study demonstrates that the presence of F. perrara influences gut immunity and homeostasis in the pylorus. This may have implications for bee health, because F. perrara prevalence differs between colonies and increased abundance of this bacterium has been shown to correlate with dietary alteration and impaired host development. Our transcriptome analysis sets the groundwork for investigating the interplay of bee gut symbionts with the host immune system.
The evolution of sex chromosomes involves the suppression of recombination around a sexdetermining locus, and the subsequent divergence in DNA sequence between the two homologous sex chromosomes. Dioecious plants offer the opportunity to study independent early stages of this process, because of multiple, recent transitions between hermaphroditism and dioecy. Here, we present data from de novo genome assembly and annotation, genetic mapping and transcriptome analysis of the diploid dioecious herb Mercurialis annua, revealing several of the typical hallmarks of early sex-chromosome evolution. Until now only a single sex-linked PCR marker has been published. Our analysis identified a single linkage group, LG10, as the likely sex chromosome, with a region containing 69 sex-linked transcripts with a clearly lower male than female recombination, high X/Y divergence and multiple incidences of premature stop codons on the Y allele. We found many genes with sexbiased expression. Female-biased genes were randomly distributed across the genome, but male-biased genes were slightly enriched on the Y chromosome. Interestingly, Y-linked genes had reduced expression compared with X-linked genes, a pattern consistent with Y chromosome degeneration. M. annua has been a powerful model for the study of rapid sexualsystem transitions in plants; our results here establish it as a model for the study of the early stages of sex-chromosome evolution.
Bacteria that engage in long-standing associations with particular hosts are expected to evolve host-specific adaptations that limit their capacity to thrive in other environments. Consistent with this, many gut symbionts seem to have a limited host range, based on community profiling and phylogenomics. However, few studies have experimentally investigated host specialization of gut symbionts and the underlying mechanisms have largely remained elusive. Here, we studied host specialization of a dominant gut symbiont of social bees, Lactobacillus Firm5. We show that Firm5 strains isolated from honey bees and bumble bees separate into deep-branching host-specific phylogenetic lineages. Despite their divergent evolution, colonization experiments show that bumble bee strains are capable of colonizing the honey bee gut. However, they were less successful than honey bee strains, and competition with honey bee strains completely abolished their colonization. In contrast, honey bee strains of divergent phylogenetic lineages were able to coexist within individual bees. This suggests that both host selection and interbacterial competition play important roles in host specialization. Using comparative genomics of 27 Firm5 isolates, we found that the genomes of honey bee strains harbour more carbohydrate-related functions than bumble bee strains, possibly providing a competitive advantage in the honey bee gut. Remarkably, most of the genes encoding carbohydrate-related functions were not conserved among the honey bee strains, which suggests that honey bees can support a metabolically more diverse community of Firm5 strains than bumble bees. These findings advance our understanding of the genomic changes underlying host specialization.
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