An official website of the United States government
ABSTRACT Microbial dispersal is essential for establishment in new habitats, but the role of vector identity is poorly understood in community assembly and function. Here, we compared microbial assembly and function in floral nectar visited by legitimate pollinators (hummingbirds) and nectar robbers (carpenter bees). We assessed effects of visitation on the abundance and composition of culturable bacteria and fungi and their taxonomy and function using shotgun metagenomics and nectar chemistry. We also compared metagenome-assembled genomes (MAGs) of Acinetobacter, a common and highly abundant nectar bacterium, among visitor treatments. Visitation increased microbial abundance, but robbing resulted in 10× higher microbial abundance than pollination. Microbial communities differed among visitor treatments: robbed flowers were characterized by predominant nectar specialists within Acetobacteraceae and Metschnikowiaceae, with a concurrent loss of rare taxa, and these resulting communities harbored genes relating to osmotic stress, saccharide metabolism and specialized transporters. Gene differences were mirrored in function: robbed nectar contained a higher percentage of monosaccharides. Draft genomes of Acinetobacter revealed distinct amino acid and saccharide utilization pathways in strains isolated from robbed versus pollinated flowers. Our results suggest an unrecognized cost of nectar robbing for pollination and distinct effects of visitor type on interactions between plants and pollinators. Overall, these results suggest vector identity is an underappreciated factor structuring microbial community assembly and function.
more »
« less
Culturable bacteria are more common than fungi in floral nectar and are more easily dispersed by thrips, a ubiquitous flower visitor
ABSTRACT Variation in dispersal ability among taxa affects community assembly and biodiversity maintenance within metacommunities. Although fungi and bacteria frequently coexist, their relative dispersal abilities are poorly understood. Nectar-inhabiting microbial communities affect plant reproduction and pollinator behavior, and are excellent models for studying dispersal of bacteria and fungi in a metacommunity framework. Here, we assay dispersal ability of common nectar bacteria and fungi in an insect-based dispersal experiment. We then compare these results with the incidence and abundance of culturable flower-inhabiting bacteria and fungi within naturally occurring flowers across two coflowering communities in California across two flowering seasons. Our microbial dispersal experiment demonstrates that bacteria disperse via thrips among artificial habitat patches more readily than fungi. In the field, incidence and abundance of culturable bacteria and fungi were positively correlated, but bacteria were much more widespread. These patterns suggest shared dispersal routes or habitat requirements among culturable bacteria and fungi, but differences in dispersal or colonization frequency by thrips, common flower visitors. The finding that culturable bacteria are more common among nectar sampled here, in part due to superior thrips-mediated dispersal, may have relevance for microbial life history, community assembly of microbes, and plant–pollinator interactions.
more »
« less
- Award ID(s):
- 1846266
- PAR ID:
- 10380542
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- FEMS Microbiology Ecology
- Volume:
- 97
- Issue:
- 12
- ISSN:
- 1574-6941
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT Plant–microbe associations are ubiquitous, but parsing contributions of dispersal, host filtering, competition and temperature on microbial community composition is challenging. Floral nectar‐inhabiting microbes, which can influence flowering plant health and pollination, offer a tractable system to disentangle community assembly processes. We inoculated a synthetic community of yeasts and bacteria into nectars of 31 plant species while excluding pollinators. We monitored weather and, after 24 h, collected and cultured communities. We found a strong signature of plant species on resulting microbial abundance and community composition, in part explained by plant phylogeny and nectar peroxide content, but not floral morphology. Increasing temperature reduced microbial diversity, while higher minimum temperatures increased growth, suggesting complex ecological effects of temperature. Consistent nectar microbial communities within plant species could enable plant or pollinator adaptation. Our work supports the roles of host identity, traits and temperature in microbial community assembly, and indicates diversity–productivity relationships within host‐associated microbiomes.more » « less
-
Abstract Floral nectar, an important resource for pollinators, is inhabited by microbes such as yeasts and bacteria, which have been shown to influence pollinator preference. Dynamic and complex plant-pollinator-microbe interactions are likely to be affected by a rapidly changing climate, as each player has their own optimal growth temperatures and phenological responses to environmental triggers, such as temperature. To understand how warming due to climate change is influencing nectar microbial communities, we incubated a natural nectar microbial community at different temperatures and assessed the subsequent nectar chemistry and preference of the common eastern bumble bee, Bombus impatiens . The microbial community in floral nectar is often species-poor, and the cultured Brassica rapa nectar community was dominated by the bacterium Fructobacillus . Temperature increased the abundance of bacteria in the warmer treatment. Bumble bees preferred nectar inoculated with microbes, but only at the lower, ambient temperature. Warming therefore induced an increase in bacterial abundance which altered nectar sugars and led to significant differences in pollinator preference.more » « less
-
null (Ed.)Flowers at times host abundant and specialized communities of bacteria and fungi that influence floral phenotypes and interactions with pollinators. Ecological processes drive variation in microbial abundance and composition at multiple scales, including among plant species, among flower tissues, and among flowers on the same plant. Variation in microbial effects on floral phenotype suggests that microbial metabolites could cue the presence or quality of rewards for pollinators, but most plants are unlikely to rely on microbes for pollinator attraction or reproduction. From a microbial perspective, flowers offer opportunities to disperse between habitats, but microbial species differ in requirements for and benefits received from such dispersal. The extent to which floral microbes shape the evolution of floral traits, influence fitness of floral visitors, and respond to anthropogenic change is unclear. A deeper understanding of these phenomena could illuminate the ecological and evolutionary importance of floral microbiomes and their role in the conservation of plant–pollinator interactions.more » « less
-
Abstract Floral microbes, including bacteria and fungi, alter nectar quality, thus changing pollinator visitation. Conversely, pollinator visitation can change the floral microbial community.Most studies on dispersal of floral microbes have focused on bees, ants or hummingbirds, yet Lepidoptera are important pollinators.We asked (a) where are microbes present on the butterfly body, (b) do butterflies transfer microbes while foraging, and (c) how does butterfly foraging affect microbial abundance on different floret structures.The tarsi and proboscis had significantly more microbes than the thorax in wild‐caughtGlaucopsyche lygdamus(Lepidoptera: Lycaenidae) andSpeyeria mormonia(Lepidoptera: Nymphalidae).Glaucopsyche lygdamus, a smaller‐bodied species, had fewer microbes thanS. mormonia.As a marker for microbes, we used a bacterium (Rhodococcus fascians,near NCBI Y11196) isolated from aS. mormoniathat was foraging for nectar, and examined its dispersal byG. lygdamusandS. mormoniavisiting florets ofPyrrocoma crocea(Asteraceae). Microbial dispersal among florets correlated positively with bacterial abundance in the donor floret. Dispersal also depended on butterfly species, age, and bacterial load carried by the butterfly.Recipient florets had less bacteria than donor florets. The nectaries had more bacteria than the anthers or the stigmas, while anthers and stigmas did not differ from each other. There was no differential transmission among floral organs.Lepidoptera thus act as vectors of floral microbes. Including Lepidoptera is thus crucial to an understanding of plant–pollinator–microbe interactions. Future studies should consider the role of vectored microbes in lepidopteran ecology and fitness.more » « less
