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The Shared Microbiome of Bees and Flowers

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The Shared Microbiome of Bees and Flowers Available online at www.sciencedirect.com ScienceDirect (More than) Hitchhikers through the network: The shared microbiome of bees and flowers 1,2,8 3,8 Alexander Keller , Quinn S McFrederick , 4 4,5 6 Prarthana Dharampal , Shawn Steffan , Bryan N Danforth and 7 Sara D Leonhardt Growing evidence reveals strong overlap between production, biodiversity, and ecosystem functions. There- microbiomes of flowers and bees, suggesting that flowers are fore, hubs of microbial transmission. Whether floral transmission is pollination is an intensively studied research field. One the main driver of bee microbiome assembly, and whether emerging facet is the interaction of bees and plants with functional importance of florally sourced microbes shapes bee microbes [1,2]. Microbes can contribute positively or nega- foraging decisions are intriguing questions that remain tively to host health, development and fecundity.Detrimen- unanswered. We suggest that interaction network properties, tal effects on bees and plants are caused by pathogens and such as nestedness, connectedness, and modularity, as well competitors, while beneficial symbionts affect nutrition, as specialization patterns can predict potential transmission detoxification, and pathogen defense [1,2]. Insights into routes of microbes between hosts. Yet microbial filtering by the occurrence, nature, and implications of these associations plant and bee hosts determines realized microbial niches. strongly contribute to our understanding of the current risk Functionally, shared floral microbes can provide benefits for factors threatening bee and plant populations. bees by enhancing nutritional quality, detoxification, and disintegration of pollen. Flower microbes can also alter the Microbe-host associations in pollination systems are how- attractiveness of floral resources. Together, these mechanisms ever not isolated, but embedded in complex and multi- may affect the structure of the flower-bee interaction network. layered interaction networks [3,4]. New insights propose a dynamic and variable system of microbial associations, Addresses where the structure of the pollination network may be a 1 Department of Bioinformatics, Biocenter, University of Wu¨ rzburg, main determinant of microbial dispersal routes [5 ]. Flower 97074, Wu¨ rzburg, Germany 2 microbes can contribute to large proportions of microbiomes Center for Computational and Theoretical Biology, Biocenter, in dietary provisions stored in nests and larval guts of bees, University of Wu¨ rzburg, 97074 Wu¨ rzburg, Germany 3 Department of Entomology, University of California, Riverside, particularly insolitarybee species [6].Bees can thus establish Riverside, CA 92501, USA microbial associations from environmental, particularly flo- 4 Department of Entomology, University of Wisconsin-Madison, ral, sources by foraging [7]. Also, microbes classified as bee- Madison, WI 53706, USA 5 adapted were found in flowers [8], which can in turn serve as USDA-ARS, Vegetable Crops Research Unit, Madison, Wisconsin, USA 6 intermediary transmission hubs facilitating intra- and inter- Department of Entomology, Cornell University, Ithaca, NY 14850, USA 7 Department of Life Science Systems, School of Life Sciences, specific microbial exchange [8]. Consequently, microbes are Technical University of Munich, 85354 Freising, Germany vectored between flowers by pollinators, and this give-and- take of microbes can also shape floral microbiomes. Micro- Corresponding author: bial associations in the pollination system thus have an Keller, Alexander ([email protected]) 8 Shared first authors. underlying meta-community structure [9 ], affected by interactions between their respective hosts. Current Opinion in Insect Science 2021, 44:xx–yy This review comes from a themed issue on Ecology On the other hand, it is unlikely that network structure is the sole driver of microbial community assembly, since Edited by Rachel Vannette and Robert R Junker hosts nevertheless uphold distinctive microbiome ele- ments despite their connectivity in the overall network [2,5 ,10]. Host traits can determine which microbes are https://doi.org/10.1016/j.cois.2020.09.007 transferred, establish and proliferate, not only between interacting bees and flowers, but also between individuals 2214-5745/ã 2020 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons. or species on the same side of the network. In this review, org/licenses/by/4.0/). we highlight current literature on bee and flower micro- biomes with special emphasis on the role of local network structure for microbe sharing, evolutionary predisposition Introduction and relevant microbe and host traits. Bee-plant associations are crucial for most terrestrial natural and agricultural systems as they maintain primary www.sciencedirect.com Current Opinion in Insect Science 2021, 44:1–8 2 Ecology Multidirectional microbial transmission is Plant-pollinator network characteristics, however, can central in plant-bee interaction networks vary within and between habitats. For example, while During prolonged floral visitation trips, foraging bees all communities in Andean plant-pollinator communities leave behind microbes passively by sloughing of propa- (Table S1) exhibited significant nestedness and modular- gules from the integument, or actively by feeding and ity, nestedness decreased and modularity increased with defecation [11]. Recent studies investigating floral micro- altitude in Chile [20]. As a consequence of greater shared biomes reported microbes usually attributed to bees or flower visitation, microbiomes across bee species may be other insects, such as Apilactobacillus and Bifidobacterium more homogeneous at lower altitudes. At higher altitudes, [8,12,13], although visitation by bees does not appear as increased network modularity may lead to greater modu- the exclusive transmission pathway for these bacteria [8]. larity also in bee-related and floral microbiomes across These microbes occurred in lower abundances in flowers specialized and generalized host species. In general, more than in bees, suggesting that they are better adapted to emphasis should be given to how diversity and distribu- and more active in bee guts than in flowers, but do have tion of microbes across bees and flowering plants are characteristics that enable them to persist in both envir- related to modularity, nestedness and habitat-specific onments [8]. With bees eating pollen, drinking nectar or differences in interaction networks. Recently, Zemenick storing these resources in the nest, floral microbes and colleagues [5 ] used coupled plant-pollinator and become a central part of the nest environment and are plant-microbe networks to show that a plant’s position in taken up by adults and larvae [14,15]. The interaction a pollination network influences, but does not fully between bees and plants is thus recognized as a general explain, the composition of its floral microbiome. Intro- transmission route for microbes in both directions. In duced microbes may undergo a process of ’filtration’ by complex networks, this reciprocal exchange can in theory the flower and resident microbes such that some microbes lead to a series of transmission events within and between are enriched, and others are inhibited. This would ulti- species given visitation of a single flower by multiple bees mately impact transmission via subsequent visitors [5 ]. and foraging of individual bees on multiple flowers [8,16,17 ]. Such microbiome homogenization may explain The degree of specialization can shape why pollen microbiomes of insect-pollinated plant spe- microbial transmission networks cies were more similar than those of wind-pollinated While it is tempting to assume that specialist (oligolectic) plants [16]. bees will have different (i.e. more specialized) microbes than generalist (polylectic) floral visitors, known pollina- tion network structures do not entirely support this Local network architecture determines assumption. Depending on the degree of nestedness potential dispersal routes and the local network structure, specialized oligolectic While the architecture of mutualistic plant-pollinator bees may rather have microbiomes which represent a networks is well studied, we hardly know how this archi- subset of those found in more generalized polylectic bees; tecture affects transmission of microbes. Pollination net- and the same may hold true for specialist and generalist works are mostly non-random with a predominantly plants. Nonetheless, taxonomic specialization of bees on nested architecture, i.e. rare (specialized) bees visit com- specific plant partners can narrow down potential trans- mon (generalized) plants and rare (specialized) plants are mission links for microbes, particularly by contributing to visited by common (generalized) bees [18]. Modularity modularity in networks. (exclusive network subsets with dense interactions) increases with species richness [19]. This typical structure Narrow host-plant associations and constrained floral vis- of local pollination networks has direct implications on itation patterns could in theory be a strategy to addition- the transfer of microbes; without any filtering mecha- ally ensure recruitment of beneficial microbes for each nisms preventing microbial transmission, the default pre- new generation of bees. Due to co-evolution, floral micro- diction would be high microbiome overlap for bee-plant bial communities of particular plant species or families are networks
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