Current European Labyrinthula zosterae Are Not Virulent and Modulate Seagrass (Zostera marina) Defense Gene Expression

Abstract

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.

Functional, Phylogenetic and Host-Geographic Signatures of Labyrinthula spp. Provide for Putative Species Delimitation and a Global-Scale View of Seagrass Wasting Disease

“…This could be due to any number of factors (e.g., differing plant genetics or condition within and among experiments, or changing pathogen condition over time). However, this species can be present in both green and lesioned leaves, and may modulate host immunity (Brakel et al 2014). Additionally, our cross-host infection experiments indicate at least the possibility for some Labyrinthula, such as our isolate 8b (haplotype 8, species E), to become novel pathogens (e.g., in Z. marina or P. oceanica beds), though 8b's reduced virulence on species like Z. marina (this study) might equally argue against it causing epidemics as such an invasive.…”

“…Neither of these studies nor the study that provided the original 18S rDNA identification of L. zosterae (Leander and Porter 2001) paired sequencing directly with pathogenicity testing for their isolates. However, Brakel et al (2014) did pair geographically based isolate assays and sequencing, but specifically for L. zosterae and only within European eelgrass beds. Thus, at the time of this analysis, the only studies to couple broader assays (across-host-species and large geographic ranges) of isolate pathogenicity with molecular identification are from terrestrial systems, which suggest a hidden diversity of pathogenic and non-pathogenic Labyrinthula for Poaceae hosts (Craven et al 2005;Douhan et al 2009).…”

Marine Phytophthora species can hamper conservation and restoration of vegetated coastal ecosystems

“…Although L. zosterae has been shown to be able to cause wasting disease symptoms [58], not all species from the Labyrinthula genus are pathogenic [59]. Indeed, recent work has shown that current isolates from European Z. marina populations display varying virulence [60,61], and Labyrinthula spp. seem to be very common in northern Z. marina beds [62].…”

Climate Change Impacts on Seagrass Meadows and Macroalgal Forests: An Integrative Perspective on Acclimation and Adaptation Potential

“…Although macroalgae and seagrasses form habitats worldwide known as hotspots of biodiversity and production, we know little about the microbes in these ecosystems (Bengtsson et al, 2012), but see Clasen and Shurin (2015) for an ecosystem approach. The relative few microbial studies performed have focused almost exclusively on (epi-)bacterial communities associated to seagrasses and macroalgae, neglecting most other microbes (Bengtsson et al, 2012;Bockelmann et al, 2012Bockelmann et al, , 2013Michelou et al, 2013;Brakel et al, 2014Brakel et al, , 2017Cúcio et al, 2016;Singh and Reddy, 2016). On top of that, particularly functional interactions between marine macrophytes and their microbiomes are poorly known.…”