Modulation of the Eelgrass – Labyrinthula zosterae Interaction Under Predicted Ocean Warming, Salinity Change and Light Limitation

Janina Brakel,Anna-Christina Bockelmann,Thorsten B H Reusch,Stina Jakobsson-Thor

doi:10.3389/fmars.2019.00268

Janina Brakel, Anna-Christina Bockelmann + Show 2 more

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https://doi.org/10.3389/fmars.2019.00268

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Abstract

Marine infectious diseases can have large-scale impacts when they affect foundation species such as seagrasses and corals. Interactions between host and disease, in turn, may be modulated by multiple perturbations associated with global change. A case in point is the infection of the foundation species Zostera marina (eelgrass) with endophytic net slime molds (Labyrinthula zosterae), the putative agent of eelgrass wasting disease that caused one of the most severe marine pandemics across the North-Atlantic in the 1930s. The contemporary presence of L. zosterae in many eelgrass meadows throughout Europe raises the question whether such a pandemic may re-appear if coastal waters become more eutrophic, warmer and less saline. Accordingly, we exposed uninfected Baltic Sea Z. marina plants raised from seeds to full factorial combinations of controlled L. zosterae inoculation, heat stress, light limitation (mimicking one consequence of eutrophication) and two salinity levels. We followed eelgrass wasting disease dynamics, along with several eelgrass responses such as leaf growth, mortality and carbohydrate storage, as well as the ability of plants to chemically inhibit L. zosterae growth. Contrary to our expectation, inoculation with L. zosterae reduced leaf growth and survival only under the most adverse condition to eelgrass (reduced light and warm temperatures). We detected a strong interaction between salinity and temperature on L. zosterae abundance and pathogenicity. The protist was unable to infect eelgrass under high temperature (27°C) in combination with low salinity (12 psu). With the exception of a small positive effect of temperature alone, no further effects of any of the treatment combinations on the defense capacity of eelgrass against L. zosterae were detectable. This work supports the idea that contemporary L. zosterae isolates neither represent an immediate risk for eelgrass beds in the Baltic Sea, nor a future one under the predicted salinity decrease and warming of the Baltic Sea.

Highlights

Environmental stressors may change complex species interactions resulting in broad ecological restructuring (Araújo and Luoto, 2007; Tylianakis et al, 2008; Van der Putten et al, 2010; Yang and Rudolf, 2010)
In order to assess the infection success and the ability to produce disease symptoms under different environmental treatments, we evaluated L. zosterae cell numbers in leaf tissue in parallel with the measurement wasting disease symptoms on inoculated leaves 2 and 8 days post inoculation
To the best of our knowledge, this is the first controlled infection study that used naive plants raised from seeds and a thorough quantification using RT-qPCR to control sham infection, as well as the progression of L. zosterae in planta, in combination with three fully orthogonal stressors

Summary

Introduction

Environmental stressors may change complex species interactions resulting in broad ecological restructuring (Araújo and Luoto, 2007; Tylianakis et al, 2008; Van der Putten et al, 2010; Yang and Rudolf, 2010). It has been argued that disease prevalence will increase under progressive severity of global change (Harvell et al, 1999, 2002) Under this scenario, commensals and opportunistic pathogens are more likely to cause a disease because either the host immune competence is compromised, and/or pathogen reproduction rates increase (Burge et al, 2013). For most marine host–pathogen systems the influence of environmental factors is unresolved This applies to the seagrass – ‘wasting disease’ interaction, where species of marine flowering plants are infected by a colonial protist species belonging to the Stramenopiles (Labyrinthulidae, net slime molds). Lesions were later causally related to an infection by the marine net slime mold Labyrinthula zosterae (Short et al, 1987; Muehlstein et al, 1988). L. zosterae and other Labyrinthula spp. are endophytes that inhabit leaves of various seagrass species (Martin et al, 2016), feeding on plant cell organelles by osmotrophy (Muehlstein, 1992; Raghukumar, 2002)

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