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ABSTRACT Coupling remote sensing with microbial omics-based approaches provides a promising new frontier for scientists to scale microbial interactions across space and time. These data-rich, interdisciplinary methods allow us to better understand interactions between microbial communities and their environments and, in turn, their impact on ecosystem structure and function. Here, we highlight current and novel examples of applying remote sensing, machine learning, spatial statistics, and omics data approaches to marine, aquatic, and terrestrial systems. We emphasize the importance of integrating biochemical and spatiotemporal environmental data to move toward a predictive framework of microbiome interactions and their ecosystem-level effects. Finally, we emphasize lessons learned from our collaborative research with recommendations to foster productive and interdisciplinary teamwork.

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 andmore »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.« less

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 fastermore »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.« less

The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth’s ecosystems.