Abstract

The temperate seagrass species eelgrass Zostera marina can be infected by the wasting disease pathogen Labyrinthula zosterae, which is believed to have killed about 90% of the seagrass in the Atlantic Ocean in the 1930s. It is not known why this opportunistic pathogen sometimes becomes virulent, but the recurrent outbreaks may be due to a weakening of the Z. marina plants from adverse environmental changes. This study investigated the individual and interactive effects of multiple extrinsic factors (temperature, light, and tissue damage) on the host-pathogen interaction between Z. marina and L. zosterae in a fully crossed infection experiment. The degree of infection was measured as both lesion coverage and L. zosterae cell concentration. We also investigated if the treatment factors affect the chemical defense of the host, measured as the inhibitory capacity of seagrass extracts in bioassays with L. zosterae. Finally, gene expression of a set of targeted genes was quantified in order to investigate how the treatments change Z. marina’s response to infection. Light had a pronounced effect on L. zosterae infection measured as lesion coverage, where reduced light conditions increased lesions by 35%. The response to light on L. zosterae cell concentration was more complex and showed significant interaction with the temperature treatment. Cell concentration was also significantly affected by physical damage, where damage surprisingly resulted in a reduced cell concentration of the pathogen. No treatment factor caused detectable decrease in the inhibitory capacity of the seagrass extracts. There were several interactive effects between L. zosterae infection and the treatment factors on Z. marina growth, and on the expression of genes associated with immune defense, phenol synthesis and primary metabolism, showing that the molecular reaction towards L. zosterae infection depends on prevailing environmental conditions. Our study shows that individual or interactive effects of light, temperature and tissue damage can affect multiple aspects of host-pathogen interactions in seagrass. These results highlights the complexity of marine host-pathogen systems, showing that more multi-factorial investigations are needed to gain a better understanding of disease in marine plants under different environmental conditions.

Highlights

  • Seagrass meadows are habitats dominated by one or several species of seagrasses, and they constitute one of the most important types of coastal marine ecosystems globally (Costanza et al, 2014)

  • All Z. marina shoots developed lesions when inoculated with L. zosterae cells, whereas no lesions were detected on noninoculated shoots

  • We show that changes in extrinsic factors can have an impact on the host-pathogen interaction on a relatively short time scale

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Summary

Introduction

Seagrass meadows are habitats dominated by one or several species of seagrasses, and they constitute one of the most important types of coastal marine ecosystems globally (Costanza et al, 2014). The meadows act as nursery grounds for commercially important fish and shellfish species (Orth et al, 1984), function as coastal protection (Barbier et al, 2011), and sequester large amounts of carbon (Duarte et al, 2005). During the last decades seagrass populations have declined sharply worldwide (Waycott et al, 2009), due to multiple stressors such as sediment and nutrient runoff, physical disturbance, invasive species, commercial fishing practices, aquaculture, overgrazing, algal blooms, global warming, and disease (Orth et al, 2006). The pathogen is a colonyforming stramenopile that causes black necrotic lesions on its host plant, and is likely the causative organism responsible the wasting disease outbreaks in the 1930s, when about 90% of the Atlantic populations of Z. marina vanished over a span of a few years (reviewed by Sullivan et al, 2013). Stressors caused by a changing environment, e.g., heat stress, reduced light and salinity, and lowered pH, are all factors that potentially can increase pathogen susceptibility of an organism (Chakraborty et al, 2000; Anderson et al, 2004)

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