Comparative metagenomics reveals expanded insights into intra- and interspecific variation among wild bee microbiomes

Abstract

The holobiont approach proposes that species are most fully understood within the context of their associated microbiomes, and that both host and microbial community are locked in a mutual circuit of co-evolutionary selection. Bees are an ideal group for this approach, as they comprise a critical group of pollinators that contribute to both ecological and agricultural health worldwide. Metagenomic analyses offer comprehensive insights into an organism’s microbiome, diet, and viral load, but remain largely unapplied to wild bees. Here, we present metagenomic data from three species of carpenter bees sampled from around the globe, representative of the first ever carpenter bee core microbiome. Machine learning, co-occurrence, and network analyses reveal that wild bee metagenomes are unique to host species. Further, we find that microbiomes are likely strongly affected by features of their local environment, and feature evidence of plant pathogens previously known only in honey bees. Performing the most comprehensive comparative analysis of bee microbiomes to date we discover that microbiome diversity is inversely proportional to host species social complexity. Our study helps to establish some of the first wild bee hologenomic data while offering powerful empirical insights into the biology and health of vital pollinators.

Characterisation of the gut bacteriome of hill and plain race of Indian honey bee <i>Apis cerana</i> fabricius

“…Prevalence of Pseudomonas has been observed in the Hill race honey bees gut microflora, which was found to have an important role in the spread of plant pathogens which causes plant diseases (Pattemore et al, 2014;Anjum et al, 2021). In addition, reports on the whole microbiome also dictate the same observation, where Pseudomonas SPS is being harbored by the carpenter bees (Subotic et al, 2019) and wild bees (Shell and Rehan, 2022).…”

The effects of urban land use gradients on wild bee microbiomes

“…Bacteria of the genus Sphingomonas have been shown to be negatively correlated with Fusarium species that cause Fusarium Head Blight in maize crops (Cobo-Díaz et al, 2019). In C. calcarata, Sphingomonas co-occurred positively with the fungal genera Pantoea (Nguyen and Rehan, 2022), a genus prevalent in C. australensis (Shell and Rehan, 2022), A. mellifera (Wright et al, 2001), and stingless bees (Leonhardt and Kaltenpoth, 2014). Additionally, Sphingomonas is a dominant bacteria found in the nests of stingless bees Frieseomelitta varia, Melipona quadrifasciata, and Tetragonisca angustula (de Sousa, 2021) and is also found in A. mellifera (Anjum et al, 2018;Muñoz-Colmenero et al, 2020) and O. bicornis microbiomes (Mohr and Tebbe, 2006), thus this bacteria co-occurs naturally with wild bees.…”

“…For solitary wild bees, this research is in its infancy; however, it is known that wild bees do not always maintain the same consistent core microbiome seen in social bees ( McFrederick et al, 2012 , 2014 ; Kwong and Moran, 2016 ; McFrederick and Rehan, 2016 ; Graystock et al, 2017 ). An example on how solitary wild bees can have differing core microbiomes can be found in C. calcarata , a wild bee displaying different core microbiomes from other bee species and across different regions ( Graystock et al, 2017 ; Dew et al, 2020 ; Nguyen and Rehan, 2022 ; Shell and Rehan, 2022 ).…”

“…Sociality can influence the bee microbiome by impacting how solitary and social bees interact with food resources, the environment, and other bees to transmit different microbes ( Mohr and Tebbe, 2006 ). Across various bee species, environmental factors such as climate ( McFrederick and Rehan, 2019 ), agriculture ( Motta et al, 2018 ; Muñoz-Colmenero et al, 2020 ), natural habitat, floral resources, and wild bee diversity in the landscape can all shape microbe composition ( Cohen et al, 2020 ; Shell and Rehan, 2022 ). In previous studies of Osmia lignaria, the presence of some microbes, such as Apilactobacillus sp., was associated with increased green spaces and an increased relative rarified ASV abundance in bees from less developed landscapes as opposed to urban and highly developed sites ( Cohen et al, 2020 ).…”

“…Numerous studies have characterized diversity and composition of the microbiome and pollen provisions in C. calcarata ( McFrederick and Rehan, 2016 ; Graystock et al, 2017 ; Dew et al, 2020 ; Nguyen and Rehan, 2022 ). In adult bees this core microbiome consists of 13 bacterial phylotypes, including Lactobacillus, Acinetobacter, Methylobacterium, Pseudomonas, and Gilliamella ( Graystock et al, 2017 ; Shell and Rehan, 2022 ), several of which are common in other bee microbiomes as well ( Vásquez et al, 2012 ; Voulgari-Kokota et al, 2019 ; Kapheim et al, 2021 ). The C. calcarata fungal microbiome includes members such as Alternaria, Ascosphaera and Penicillium ( Nguyen and Rehan, 2022 ).…”