skip to main content


This content will become publicly available on August 23, 2024

Title: 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 ofEpilobium 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
Award ID(s):
2109460
NSF-PAR ID:
10467797
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
New Phytologist
Volume:
240
Issue:
3
ISSN:
0028-646X
Format(s):
Medium: X Size: p. 1233-1245
Size(s):
["p. 1233-1245"]
Sponsoring Org:
National Science Foundation
More Like this
  1. 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
  2. Abstract

    Freshwater mussels are important for nutrient cycling and ecosystem health as they filter feed on their surrounding water. This filter feeding makes these bivalves especially sensitive to conditions in their environment. Gut microbial communities (microbiomes) have been recognised as important to both host organism and ecosystem health; however, how freshwater mussel microbiomes are organised and influenced is unclear.

    In this study, the gut bacterial microbiome of Threeridge mussel,Amblema plicata, was compared across two river basins, five rivers, and nine local sites in the south‐eastern U.S.A. Mussel gut tissue was dissected, DNA extracted, and the microbiome characterised by high throughput sequencing of the V4 region of the 16S ribosomal RNA gene.

    Planctomycetes, Firmicutes, and Cyanobacteria were the most common bacterial phyla within the guts of all sampledA.plicata. However, the relative abundances of these major bacterial phyla differed between mussels sampled from different rivers and river basins, as did the relative abundance of specific bacterial operational taxonomic units (OTUs). Despite these differences, a core microbiome was identified across all mussels, with eight OTUs being consistent members of theA.plicatamicrobiome at all sites, the most abundant OTU identifying as a member of the family Planctomycetaceae. Geographic distance between sites was not correlated with similarity in the structure of the gut microbiome, which was more related to site physicochemistry.

    Overall, these results suggest that while physicochemical conditions affect the composition of transient bacteria in the Threeridge mussel gut microbiome, the core microbiome is largely unaffected, and a portion of theA.plicatamicrobiome is retained regardless of the river system.

    How long transient bacteria remain in the gut, and to what extent these transient microbes aid in host function is still unknown. Core microbiota have been found to aid in multiple functions within animal hosts, and within freshwater mussels this core microbiome may aid in nutrient processing and cycling. Therefore, it is important to look at both transient and core microbes when studying the structure of freshwater invertebrate microbiomes.

     
    more » « less
  3. 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
  4. Summary

    Colonization by foliar endophytic fungi can affect the expression of host plant defenses and other ecologically important traits. However, whether endophyte colonization affects the uptake or redistribution of resources within and among host plant tissues remains unstudied.

    We inoculated leaves ofTheobroma cacaowith four common colonizers that range in their effect from protective to pathogenic (Colletotrichum tropicale,Pestalotiopsissp.,Colletotrichum theobromicola, orPhytophthora palmivora). We pulsed the soil with nitrogen‐15 (15N) and then traced15N uptake and its subsequent distribution to whole plants and individual leaves.

    At a whole‐plant level,C. tropicale‐inoculated plants showed significantly greater15N uptake than endophyte‐free plants did in the same pot. Among leaves within plants, younger leaves were particularly enriched in15N, but endophyte inoculation at the individual leaf level did not alter15N distribution within plants. However, leaves co‐inoculated with pathogenicPhytophthoraand protectiveC. tropicaleexperienced significantly elevated15N content as pathogen damage increased, compared with leaves inoculated only with the pathogen. Further, endophyte–pathogen co‐infection also increased total plant biomass.

    Our results indicate that colonization by foliar endophytes significantly affects N uptake and distribution among and within host plants in ways that appear to be context dependent on other microbiome components.

     
    more » « less
  5. 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