An official website of the United States government
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
Intraspecific variation in realized dispersal probability and host quality shape nectar microbiomes
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.
more »
« less
- PAR ID:
- 10500935
- Publisher / Repository:
- New Phytologist Foundation
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 240
- Issue:
- 3
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- 1233 to 1245
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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 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
-
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
-
Nguyen, Nhu H (Ed.)ABSTRACT Across diverse ecosystems, bacteria and their hosts engage in complex relationships having negative, neutral, or positive interactions. However, the specific effects of leaf-associated bacterial community functions on plant growth are poorly understood. Although microbes can promote plant growth through various biochemical mechanisms, investigating the community’s functional contributions to plant growth remains to be explored. To address this gap, we characterized the relationships between bacterial community function and host plant growth in the purple pitcher plant (Sarracenia purpurea). The main aim of our research was to investigate how different bacterial community functions affect the growth and nutrient content in the plant. Previous research has suggested that microbial communities aid in prey decomposition and subsequent nutrient acquisition in carnivorous plants, includingS. purpurea. However, the specific functional roles of bacterial communities in plant growth and nutrient uptake are not well known. In this study, sterile, freshly opened pitchers were inoculated with three functionally distinct, pre-assembled bacterial communities. Bacterial community composition and function were measured over 8 weeks using physiological assays, metagenomics, and metatranscriptomics. Distinct community functions affected plant traits; a bacterial community enriched in decomposition was associated with larger leaves with almost double the biomass of control pitchers. Physiological differences in bacterial communities were supported by metatranscriptomics; for example, the bacterial community with the highest chitinase activity had greater expression of transcripts associated with chitinase enzymes. The relationship between bacterial community function and plant growth observed here indicates potential mechanisms, such as chitinase activity, for host-associated bacterial functions to support pitcher plant growth. IMPORTANCEThis study addresses a gap in understanding the relationships between bacterial community function and plant growth. We inoculated sterile, freshly opened pitcher plant leaves with three functionally distinct bacterial communities to uncover potential mechanisms through which bacterial functions support plant health and growth. Our findings demonstrate that distinct community functions significantly influence plant traits, with some bacterial communities supporting more plant growth than in control pitchers. These results highlight the ecological roles of microbial communities in plants and thus ecosystems and suggest that nutrient cycling is an important pathway through which microbes support host plant health. This research provides valuable insights into plant-microbe interactions and the effects of diverse microbial community functions.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/nph.19195
