Electronic versions

  • Deanna S Beatty
    University of California
  • Lillian R Aoki
    University of Oregon Health Sciences Center
  • Brendan Rappazzo
    Department of Computer Science
  • Chelsea Bergman
    San Diego State University
  • Lia K Domke
    College of Fisheries and Ocean Sciences
  • J Emmett Duffy
    MarineGEO Program and Smithsonian Environmental Research Centergrid.419533.9
  • Katie Dubois
    University of CaliforniaDepartment of Integrative Biology and Evolution
  • Ginny L Eckert
    College of Fisheries and Ocean Sciences
  • Carla Gomes
    Department of Computer Science
  • Olivia J Graham
    University of California, Los Angeles
  • Leah Harper
    MarineGEO Program and Smithsonian Environmental Research Centergrid.419533.9
  • C Drew Harvell
    University of California, Los Angeles
  • Timothy L Hawthorne
    Department of Sociology and College of Sciences GIS Cluster
  • Margot Hessing-Lewis
    Hakai Institute
  • Kevin Hovel
    San Diego State University
  • Zachary L Monteith
    Hakai Institute
  • Ryan S Mueller
    Department of Microbiology and Virology
  • Angeleen M Olson
    Hakai Institute
  • Carolyn Prentice
    Hakai Institute
  • Fiona Tomas
    Instituto Mediterráneo de Estudios Avanzados (CSIC-UIB)
  • Bo Yang
    Department of Urban and Regional Planning
  • John J Stachowicz
    University of California
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.

Keywords

  • Prevalence, Stramenopiles/physiology, Host-Pathogen Interactions, Zosteraceae/microbiology, Microbiota
Original languageEnglish
Pages (from-to)e0022422
JournalmSystems
Volume7
Issue number4
Early online date20 Jul 2022
DOIs
Publication statusPublished - 30 Aug 2022
Externally publishedYes
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