• Energy Research

Pro- and eukaryotic microbes associated with multi-cellular organisms are receiving increasing attention as a driving factor in ecosystems. Endophytes in plants can change host performance by altering nutrient uptake, secondary metabolite production or defense mechanisms. Recent studies detected widespread prevalence of Labyrinthula zosterae in European Zostera marina meadows, a protist that allegedly caused a massive amphi-Atlantic seagrass die-off event in the 1930's, while showing only limited virulence today. As a limiting factor for pathogenicity, we investigated genotype × genotype interactions of host and pathogen from different regions (10-100 km-scale) through reciprocal infection. Although the endophyte rapidly infected Z. marina, we found little evidence that Z. marina was negatively impacted by L. zosterae. Instead Z. marina showed enhanced leaf growth and kept endophyte abundance low. Moreover, we found almost no interaction of protist × eelgrass-origin on different parameters of L. zosterae virulence/Z. marina performance, and also no increase in mortality after experimental infection. In a target gene approach, we identified a significant down-regulation in the expression of 6/11 genes from the defense cascade of Z. marina after real-time quantitative PCR, revealing strong immune modulation of the host's defense by a potential parasite for the first time in a marine plant. Nevertheless, one gene involved in phenol synthesis was strongly up-regulated, indicating that Z. marina plants were probably able to control the level of infection. There was no change in expression in a general stress indicator gene (HSP70). Mean L. zosterae abundances decreased below 10% after 16 days of experimental runtime. We conclude that under non-stress conditions L. zosterae infection in the study region is not associated with substantial virulence.

The experiment consisted of three treatments: 0HW = no heat wave; 1HW = one single summer heat wave; and 3HW = three subsequent heat waves. In all three treatments, working with continuous flow-through of fjord water maintained the natural small-scale variability of most environmental parameters except temperature, which was adjusted to the logged thermal regime of the year 2009.

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. Supplement to: Brakel, Janina; Jakobsson-Thor, Stina; Bockelmann, Anna-Christina; Reusch, Thorsten B H (2019): Modulation of the Eelgrass – Labyrinthula zosterae Interaction Under Predicted Ocean Warming, Salinity Change and Light Limitation. Frontiers in Marine Science, 6

AbstractClimate change will not only shift environmental means but will also increase the intensity of extreme events, exerting additional stress on ecosystems. While field observations on the ecological consequences of heat waves are emerging, experimental evidence is rare, and lacking at the community level. Using a novel “near‐natural” outdoor mesocosms approach, this study tested whether marine summer heat waves have detrimental consequences for macrofauna of a temperate coastal community, and whether sequential heat waves provoke an increase or decrease of sensitivity to thermal stress. Three treatments were applied, defined and characterized through a statistical analysis of 15 years of temperature records from the experimental site: (1) no heat wave, (2) two heat waves in June and July followed by a summer heat wave in August and (3) the summer heat wave only. Overall, 50% of the species showed positive, negative or positive/negative responses in either abundance and/or biomass. We highlight four possible ways in which single species responded to either three subsequent heat waves or one summer heat wave: (1) absence of a response (tolerance, 50% of species), (2) negative accumulative effects by three subsequent heat waves (tellinid bivalve), (3) buffering by proceeding heat waves due to acclimation and/or shifts in phenology (spionid polychaete) and (4) an accumulative positive effect by subsequent heat waves (amphipod). The differential responses to single or sequential heat waves at the species level entailed shifts at the community level. Community‐level differences between single and triple heat waves were more pronounced than those between regimes with vs. without heat waves. Detritivory was reduced by the single heat wave while suspension feeding was less common in the triple heat wave regime. Critical extreme events occur already today and will occur more frequently in a changing climate, thus, leading to detrimental impacts on coastal marine systems.

AbstractPersistently high marine temperatures are escalating and threating marine biodiversity. The Baltic Sea, warming faster than other seas, is a good model to study the impact of increasing sea surface temperatures. Zostera marina, a key player in the Baltic ecosystem, faces susceptibility to disturbances, especially under chronic high temperatures. Despite the increasing number of studies on the impact of global warming on seagrasses, little attention has been paid to the role of the holobiont. Using an outdoor benthocosm to replicate near‐natural conditions, this study explores the repercussions of persistent warming on the microbiome of Z. marina and its implications for holobiont function. Results show that both seasonal warming and chronic warming, impact Z. marina roots and sediment microbiome. Compared with roots, sediments demonstrate higher diversity and stability throughout the study, but temperature effects manifest earlier in both compartments, possibly linked to premature Z. marina die‐offs under chronic warming. Shifts in microbial composition, such as an increase in organic matter‐degrading and sulfur‐related bacteria, accompany chronic warming. A higher ratio of sulfate‐reducing bacteria compared to sulfide oxidizers was found in the warming treatment which may result in the collapse of the seagrasses, due to toxic levels of sulfide. Differentiating predicted pathways for warmest temperatures were related to sulfur and nitrogen cycles, suggest an increase of the microbial metabolism, and possible seagrass protection strategies through the production of isoprene. These structural and compositional variations in the associated microbiome offer early insights into the ecological status of seagrasses. Certain taxa/genes/pathways may serve as markers for specific stresses. Monitoring programs should integrate this aspect to identify early indicators of seagrass health. Understanding microbiome changes under stress is crucial for the use of potential probiotic taxa to mitigate climate change effects. Broader‐scale examination of seagrass–microorganism interactions is needed to leverage knowledge on host–microbe interactions in seagrasses.

Supplement to: Saha, Mahasweta; Barboza, Francisco Rafael; Somerfield, Paul J; Al-Janabi, Balsam; Beck, Miriam; Brakel, Janina; Ito, Maysa; Pansch, Christian; Nascimento Schulze, Jennifer C; Jakobsson-Thor, Stina; Weinberger, Florian; Sawall, Yvonne (2020): Response of foundation macrophytes to near‐natural simulated marine heatwaves. Global Change Biology, 26(2), 417-430 Traits (with abbreviations for functional groups):Adult body size: S < 1mm, M 1–10mm, L 10–100mm, XL 100–1000mm, XXL > 1000mmGrowth form: E encrusting, M massive, B bushy, F filamentousMode of energy acquisition: A autotroph, P predator, S suspension feeder, D deposit feeder, G grazer, H heterotrophsReproduction: S solitary, C colonial 13 response variable have been measured for Fucus vesiculosus and Zostera marina. Year: 2015 Where: Kiel Outdoor BenthocosmTreatments: - Co (0HW) = ambient treatment with no heatwaves- 1HW = one summer heatwave- 3HWs = three heatwaves, 2 spring/early summer heatwavesAfter 3HW means end of the experiment.

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.