skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Manipulation of the seagrass‐associated microbiome reduces disease severity
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
Award ID(s):
2109607
PAR ID:
10485852
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
26
Issue:
2
ISSN:
1462-2912
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Raina, Jean-Baptiste (Ed.)
    ABSTRACT Predicting outcomes of marine disease outbreaks presents a challenge in the face of both global and local stressors. Host-associated microbiomes may play important roles in disease dynamics but remain understudied in marine ecosystems. Host–pathogen–microbiome interactions can vary across host ranges, gradients of disease, and temperature; studying these relationships may aid our ability to forecast disease dynamics. Eelgrass, Zostera marina , is impacted by outbreaks of wasting disease caused by the opportunistic pathogen Labyrinthula zosterae . We investigated how Z. marina phyllosphere microbial communities vary with rising wasting disease lesion prevalence and severity relative to plant and meadow characteristics like shoot density, longest leaf length, and temperature across 23° latitude in the Northeastern Pacific. We detected effects of geography (11%) and smaller, but distinct, effects of temperature (30-day max sea surface temperature, 4%) and disease (lesion prevalence, 3%) on microbiome composition. Declines in alpha diversity on asymptomatic tissue occurred with rising wasting disease prevalence within meadows. However, no change in microbiome variability (dispersion) was detected between asymptomatic and symptomatic tissues. Further, we identified members of Cellvibrionaceae, Colwelliaceae, and Granulosicoccaceae on asymptomatic tissue that are predictive of wasting disease prevalence across the geographic range (3,100 kilometers). Functional roles of Colwelliaceae and Granulosicoccaceae are not known. Cellvibrionaceae, degraders of plant cellulose, were also enriched in lesions and adjacent green tissue relative to nonlesioned leaves. Cellvibrionaceae may play important roles in disease progression by degrading host tissues or overwhelming plant immune responses. Thus, inclusion of microbiomes in wasting disease studies may improve our ability to understand variable rates of infection, disease progression, and plant survival. IMPORTANCE The roles of marine microbiomes in disease remain poorly understood due, in part, to the challenging nature of sampling at appropriate spatiotemporal scales and across natural gradients of disease throughout host ranges. This is especially true for marine vascular plants like eelgrass ( Zostera marina ) that are vital for ecosystem function and biodiversity but are susceptible to rapid decline and die-off from pathogens like eukaryotic slime-mold Labyrinthula zosterae (wasting disease). We link bacterial members of phyllosphere tissues to the prevalence of wasting disease across the broadest geographic range to date for a marine plant microbiome-disease study (3,100 km). We identify Cellvibrionaceae, plant cell wall degraders, enriched (up to 61% relative abundance) within lesion tissue, which suggests this group may be playing important roles in disease progression. These findings suggest inclusion of microbiomes in marine disease studies will improve our ability to predict ecological outcomes of infection across variable landscapes spanning thousands of kilometers. 
    more » « less
  2. Seagrass meadows provide valuable ecosystem benefits but are at risk from disease. Eelgrass ( Zostera marina ) is a temperate species threatened by seagrass wasting disease (SWD), caused by the protist Labyrinthula zosterae . The pathogen is sensitive to warming ocean temperatures, prompting a need for greater understanding of the impacts on host health under climate change. Previous work demonstrates pathogen cultures grow faster under warmer laboratory conditions and documents positive correlations between warmer ocean temperatures and disease levels in nature. However, the consequences of disease outbreaks on eelgrass growth remain poorly understood. Here, we examined the effect of disease on eelgrass productivity in the field. We coupled in situ shoot marking with high-resolution imagery of eelgrass blades and used an artificial intelligence application to determine disease prevalence and severity from digital images. Comparisons of eelgrass growth and disease metrics showed that SWD impaired eelgrass growth and accumulation of non-structural carbon in the field. Blades with more severe disease had reduced growth rates, indicating that disease severity can limit plant growth. Disease severity and rhizome sugar content were also inversely related, suggesting that disease reduced belowground carbon accumulation. Finally, repeated measurements of diseased blades indicated that lesions can grow faster than healthy tissue in situ . This is the first study to demonstrate the negative impact of wasting disease on eelgrass health in a natural meadow. These results emphasize the importance of considering disease alongside other stressors to better predict the health and functioning of seagrass meadows in the Anthropocene. 
    more » « less
  3. Abstract Temperature increases due to climate change have affected the distribution and severity of diseases in natural systems, causing outbreaks that can destroy host populations. Host identity, diversity, and the associated microbiome can affect host responses to both infection and temperature, but little is known about how they could function as important mediators of disease in altered thermal environments. We conducted an 8‐week warming experiment to test the independent and interactive effects of warming, host genotypic identity, and host genotypic diversity on the prevalence and intensity of infections of seagrass (Zostera marina) by the wasting disease parasite (Labyrinthula zosterae). At elevated temperatures, we found that genotypically diverse host assemblages had reduced infection intensity, but not reduced prevalence, relative to less diverse assemblages. This dilution effect on parasite intensity was the result of both host composition effects as well as emergent properties of biodiversity. In contrast with the benefits of genotypic diversity under warming, diversity actually increased parasite intensity slightly in ambient temperatures. We found mixed support for the hypothesis that a growth–defense trade‐off contributed to elevated disease intensity under warming. Changes in the abundance (but not composition) of a few taxa in the host microbiome were correlated with genotype‐specific responses to wasting disease infections under warming, consistent with the emerging evidence linking changes in the host microbiome to the outcome of host–parasite interactions. This work emphasizes the context dependence of biodiversity–disease relationships and highlights the potential importance of interactions among biodiversity loss, climate change, and disease outbreaks in a key foundation species. 
    more » « less
  4. Seawater temperatures are increasing, with many unquantified impacts on marine diseases. While prolonged temperature stress can accelerate host-pathogen interactions, the outcomes in nature are poorly quantified. We monitored eelgrass wasting disease (EWD) from 2013-2017 and correlated mid-summer prevalence of EWD with remotely sensed seawater temperature metrics before, during, and after the 2015-2016 marine heatwave in the northeast Pacific, the longest marine heatwave in recent history. Eelgrass shoot density declined by 60% between 2013 and 2015 and did not recover. EWD prevalence ranged from 5-70% in 2013 and increased to 60-90% by 2017. EWD severity approximately doubled each year between 2015 and 2017. EWD prevalence was positively correlated with warmer temperature for the month prior to sampling while EWD severity was negatively correlated with warming prior to sampling. This complex result may be mediated by leaf growth; bigger leaves may be more likely to be diseased, but may also grow faster than lesions, resulting in lower severity. Regional stressors leading to population declines prior to or early in the heatwave may have exacerbated the effects of warming on eelgrass disease susceptibility and reduced the resilience of this critical species. 
    more » « less
  5. Tortosa, Pablo (Ed.)
    ABSTRACT Bacteria shape interactions between hosts and fungal pathogens. In some cases, bacteria associated with fungi are essential for pathogen virulence. In other systems, host-associated microbiomes confer resistance against fungal pathogens. We studied an aphid-specific entomopathogenic fungus calledPandora neoaphidisin the context of both host and pathogen microbiomes. Aphids host several species of heritable bacteria, some of which confer resistance againstPandora. We first found that spores that emerged from aphids that harbored protective bacteria were less virulent against subsequent hosts and did not grow on plate media. We then used 16S amplicon sequencing to study the bacterial microbiome of fungal mycelia and spores during plate culturing and host infection. We found that the bacterial community is remarkably stable in culture despite dramatic changes in pathogen virulence. Last, we used an experimentally transformed symbiont of aphids to show thatPandoracan acquire host-associated bacteria during infection. Our results uncover new roles for bacteria in the dynamics of aphid-pathogen interactions and illustrate the importance of the broader microbiological context in studies of fungal pathogenesis. IMPORTANCEEntomopathogenic fungi play important roles in the population dynamics of many insect species. Understanding the factors shaping entomopathogen virulence is critical for agricultural management and for the use of fungi in pest biocontrol. We show that heritable bacteria in aphids, which confer protection to their hosts against fungal entomopathogens, influence virulence against subsequent hosts. Aphids reproduce asexually and are typically surrounded by genetically identical offspring, and thus these effects likely shape the dynamics of fungal disease in aphid populations. Furthermore, fungal entomopathogens are known to rapidly lose virulence in lab culture, complicating their laboratory use. We show that this phenomenon is not driven by changes in the associated bacterial microbiome. These results contribute to our broader understanding of the aphid model system and shed light on the biology of the Entomophthorales—an important but understudied group of fungi. 
    more » « less