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
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
- NSF-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
-
-
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‐caught
Glaucopsyche 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. mormonia that was foraging for nectar, and examined its dispersal byG. lygdamus andS. mormonia visiting 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.
-
Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by driving them to alternative states. It remains unclear if these wide-ranging consequences of priority effects can be explained systematically by a common underlying factor. Here, we identify such a factor in an empirical system. In a series of field and laboratory studies, we focus on how pH affects nectar-colonizing microbes and their interactions with plants and pollinators. In a field survey, we found that nectar microbial communities in a hummingbird-pollinated shrub, Diplacus (formerly Mimulus ) aurantiacus , exhibited abundance patterns indicative of alternative stable states that emerge through domination by either bacteria or yeasts within individual flowers. In addition, nectar pH varied among D. aurantiacus flowers in a manner that is consistent with the existence of these alternative stable states. In laboratory experiments, Acinetobacter nectaris , the bacterium most commonly found in D. aurantiacus nectar, exerted a strongly negative priority effect against Metschnikowia reukaufii , the most common nectar-specialist yeast, by reducing nectar pH. This priority effect likely explains the mutually exclusive pattern of dominance found in the field survey. Furthermore, experimental evolution simulating hummingbird-assisted dispersal between flowers revealed that M. reukaufii could evolve rapidly to improve resistance against the priority effect if constantly exposed to A. nectaris -induced pH reduction. Finally, in a field experiment, we found that low nectar pH could reduce nectar consumption by hummingbirds, suggesting functional consequences of the pH-driven priority effect for plant reproduction. Taken together, these results show that it is possible to identify an overarching factor that governs the eco-evolutionary dynamics of priority effects across multiple levels of biological organization.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
-
more » « less
Summary Epiphytic microbes frequently affect plant phenotype and fitness, but their effects depend on microbe abundance and community composition. Filtering by plant traits and deterministic dispersal‐mediated processes can affect microbiome assembly, yet their relative contribution to predictable variation in microbiome is poorly understood.
We compared the effects of host‐plant filtering and dispersal on nectar microbiome presence, abundance, and composition. We inoculated representative bacteria and yeast into 30 plants across four phenotypically distinct cultivars of
Epilobium canum . We compared the growth of inoculated communities to openly visited flowers from a subset of the same plants.There was clear evidence of host selection when we inoculated flowers with synthetic communities. However, plants with the highest microbial densities when inoculated did not have the highest microbial densities when openly visited. Instead, plants predictably varied in the presence of bacteria, which was correlated with pollen receipt and floral traits, suggesting a role for deterministic dispersal.
These findings suggest that host filtering could drive plant microbiome assembly in tissues where species pools are large and dispersal is high. However, deterministic differences in microbial dispersal to hosts may be equally or more important when microbes rely on an animal vector, dispersal is low, or arrival order is important.
