skip to main content


Title: Local environment drives rapid shifts in composition and phylogenetic clustering of seagrass microbiomes
Abstract

Plant microbiomes depend on environmental conditions, stochasticity, host species, and genotype identity. Eelgrass (Zostera marina)is a unique system for plant–microbe interactions as a marine angiosperm growing in a physiologically-challenging environment with anoxic sediment, periodic exposure to air at low tide, and fluctuations in water clarity and flow. We tested the influence of host origin versus environment on eelgrass microbiome composition by transplanting 768 plants among four sites within Bodega Harbor, CA. Over three months following transplantation, we sampled microbial communities monthly on leaves and roots and sequenced the V4–V5 region of the 16S rRNA gene to assess community composition. The main driver of leaf and root microbiome composition was destination site; more modest effects of host origin site did not last longer than one month. Community phylogenetic analyses suggested that environmental filtering structures these communities, but the strength and nature of this filtering varies among sites and over time and roots and leaves show opposing gradients in clustering along a temperature gradient. We demonstrate that local environmental differences create rapid shifts in associated microbial community composition with potential functional implications for rapid host acclimation under shifting environmental conditions.

 
more » « less
Award ID(s):
1829992
NSF-PAR ID:
10400191
Author(s) / Creator(s):
;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Scientific Reports
Volume:
13
Issue:
1
ISSN:
2045-2322
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The plant microbiome can affect host function in many ways and characterizing the ecological factors that shape endophytic (microbes living inside host plant tissues) community diversity is a key step in understanding the impacts of environmental change on these communities. Phylogenetic relatedness among members of a community offers a way of quantifying phylogenetic diversity of a community and can provide insight into the ecological factors that shape endophyte microbiomes. We examined the effects of experimental nutrient addition and herbivory exclusion on the phylogenetic diversity of foliar fungal endophyte communities of the grass speciesAndropogon gerardiiat four sites in the Great Plains of the central USA. Using amplicon sequencing, we characterized the effects of fertilization and herbivory on fungal community phylogenetic diversity at spatial scales that spanned within‐host to between sites across the Great Plains. Despite increasing fungal diversity and richness, at larger spatial scales, fungal microbiomes were composed of taxa showing random phylogenetic associations. Phylogenetic diversity did not differ systematically when summed across increasing spatial scales from a few meters within plots to hundreds of kilometers among sites. We observed substantial shifts in composition across sites, demonstrating distinct but similarly diverse fungal communities were maintained within sites across the region. In contrast, at the scale of within leaves, fungal communities tended to be comprised of closely related taxa regardless of the environment, but there were no shifts in phylogenetic composition among communities. We also found that nutrient addition (fertilization) and herbivory have varying effects at different sites. These results suggest that the direction and magnitude of the outcomes of environmental modifications likely depend on the spatial scale considered, and can also be constrained by regional site differences in microbial diversity and composition.

     
    more » « less
  2. Abstract Aim

    Roots and rhizospheres host diverse microbial communities that can influence the fitness, phenotypes, and environmental tolerances of plants. Documenting the biogeography of these microbiomes can detect the potential for a changing environment to disrupt host‐microbe interactions, particularly in cases where microbes buffer hosts against abiotic stressors. We evaluated whether root‐associated fungi had poleward declines in diversity, tested whether fungal communities in roots shifted near host plant range edges, and determined the relative importance of environmental and host predictors of root fungal community structure.

    Location

    North American plains grasslands.

    Taxon

    Foundation grasses –Andropogon gerardii, Bouteloua dactyloides, B. eriopoda, B. gracilis,andSchizachyrium scopariumand root fungi.

    Methods

    At each of 24 sites representing three replicate 17°–latitudinal gradients, we collected roots from 12 individuals per species along five transects spaced 10 m apart (40 m × 40 m grid). We used next‐generation sequencing of ITS2, direct fungal culturing from roots, and microscopy to survey fungi associated with grass roots.

    Results

    Root‐associated fungi did not follow the poleward declines in diversity documented for many animals and plants. Instead, host plant identity had the largest influence on fungal community structure. Edaphic factors outranked climate or host plant traits as correlates of fungal community structure; however, the relative importance of environmental predictors differed among plant species. As sampling approached host species range edges, fungal composition converged in similarity among individual plants of each grass species.

    Main conclusions

    Environmental predictors of root‐associated fungi depended strongly on host plant species identity. Biogeographic patterns in fungal composition suggested a homogenizing influence of stressors at host plant range limits. Results predict that communities of non‐mycorrhizal, root‐associated fungi in the North American plains will be more sensitive to future changes in host plant ranges and edaphic factors than to the direct effects of climate.

     
    more » « less
  3. Abstract

    Host‐associated microbes influence host health and function and can be a first line of defence against infections. While research increasingly shows that terrestrial plant microbiomes contribute to bacterial, fungal, and oomycete disease resistance, no comparable experimental work has investigated marine plant microbiomes or more diverse disease agents. We test the hypothesis that the eelgrass (Zostera marina) leaf microbiome increases resistance to seagrass wasting disease. From field eelgrass with paired diseased and asymptomatic tissue,16S rRNAgene amplicon sequencing revealed that bacterial composition and richness varied markedly between diseased and asymptomatic tissue in one of the two years. This suggests that the influence of disease on eelgrass microbial communities may vary with environmental conditions. We next experimentally reduced the eelgrass microbiome with antibiotics and bleach, then inoculated plants withLabyrinthula zosterae, the causative agent of wasting disease. We detected significantly higher disease severity in eelgrass with a native microbiome than an experimentally reduced microbiome. Our results over multiple experiments do not support a protective role of the eelgrass microbiome againstL. zosterae. Further studies of these marine host–microbe–pathogen relationships may continue to show new relationships between plant microbiomes and diseases.

     
    more » « less
  4. Abstract

    Experimental drought has been shown to delay the development of the root microbiome and increase the relative abundance of Actinobacteria, however, the generalizability of these findings to natural systems or other diverse plant hosts remains unknown. Bacterial cell wall thickness and growth morphology (e.g., filamentous or unicellular) have been proposed as traits that may mediate bacterial responses to environmental drivers. Leveraging a natural gradient of water‐availability across the coast redwood (Sequoia sempervirens) range, we tested three hypotheses: (a) that site‐specific water‐availability is an important predictor of bacterial community composition for redwood roots and rhizosphere soils; (b) that there is relative enrichment of Actinobacteria and other monoderm bacterial groups within the redwood microbiome in response to drier conditions; and (c) that bacterial growth morphology is an important predictor of bacteria response to water‐availability, where filamentous taxa will become more dominant at drier sites compared to unicellular bacteria. We find that both α‐ and β‐diversity of redwood bacterial communities is partially explained by water‐availability and that Actinobacterial enrichment is a conserved response of land plants to water‐deficit. Further, we highlight how the trend of Actinobacterial enrichment in the redwood system is largely driven by the Actinomycetales. We propose bacterial growth morphology (filamentous vs. unicellular) as an additional mechanism behind the increase in Actinomycetales with increasing aridity. A trait‐based approach including cell‐wall thickness and growth morphology may explain the distribution of bacterial taxa across environmental gradients and help to predict patterns of bacterial community composition for a wide range of host plants.

     
    more » « less
  5. Aim: Roots and rhizospheres host diverse microbial communities that can influence the fitness, phenotypes, and environmental tolerances of host plants. Documenting the biogeography of microbiomes can detect the potential for a changing environment to disrupt host-microbe interactions, particularly in cases where microbes, such as root-associated Ascomycota, buffer hosts against abiotic stressors. We evaluated whether root-associated fungi had poleward declines in diversity as occur for many animals and plants, tested whether microbial communities shifted near host plant range edges, and determined the relative importance of latitude, climate, edaphic factors, and host plant traits as predictors of fungal community structure. Location: North American plains grasslands Taxon: Foundation North American grass species ⎯ Andropogon gerardii, Bouteloua eriopoda, B. gracilis, B. dactyloides, and Schizachyrium scoparium and their root-associated fungi Methods: At each of 24 sites representing three replicate latitudinal gradients spanning 17° latitude, we collected roots from 12 individual plants per species along five transects spaced 10 m apart (40 m × 40 m grid). We used next-generation sequencing of the fungal ITS2 region, direct fungal culturing from roots, and microscopy to survey fungi associated with grass roots. Results: Root-associated fungi did not follow the poleward declines in diversity documented for many animals and plants. Instead, host plant identity had the largest influence on fungal community structure. Edaphic factors outranked climate or host plant traits as correlates of fungal community structure; however, the relative importance of these environmental predictors differed among plant species. As sampling approached host species range edges, fungal composition converged among individual plants of each grass species. Main conclusions: Environmental predictors of root-associated fungi depended strongly on host plant species identity. Biogeographic patterns in fungal composition suggested a homogenizing influence of stressors at host plant range limits. Results predict that communities of non-mycorrhizal, root-associated fungi in the North American plains will be more sensitive to future changes in host plant ranges and edaphic factors than to the direct effects of climate. 
    more » « less