Epiphytic and endophytic microbiome of the seagrass Zostera marina: Do they contribute to pathogen reduction in seawater?

Abstract

Seagrass ecosystems provide crucial ecosystem services for coastal environments and were shown to reduce the abundance of pathogens linked to infections in humans and marine organisms. Among several potential drivers, seagrass phenolics released into seawater have been suggested to play role in pathogen suppression, but the potential involvement of the seagrass microbiome in such effect has not been studied. Here we hypothesized that the microbiome of the eelgrass Zostera marina, especially the leaf epiphytes that are at direct interface between the seagrass host and surrounding seawater, inhibit such pathogenic microorganisms, hence, contribute to their suppression. Using a culture-dependent approach, we isolated 88 bacteria and fungi associated with the surfaces and inner tissues of the eelgrass leaves (healthy and decaying) and the roots, plus 19 strains from surrounding seawater and sediment. We first assessed the broad-spectrum antibiotic activity of microbial extracts against a large panel of common aquatic, human (fecal) and plant pathogens, and finally mined the metabolome of 88 most active extracts. The healthy leaf epibiotic bacteria, particularly Streptomyces sp. strain 131, displayed broad-spectrum and potent antibiotic activity superior to some control drugs. Gram-negative bacteria abundant on healthy leaf surfaces, and few endosphere-associated bacteria and fungi also showed remarkable antimicrobial activity. UPLC-MS/MS-based massive untargeted metabolomics analyses showed the rich specialized metabolite repertoire of strains with low annotation rates, indicating the presence of many undescribed antimicrobials in the extracts. This study contributes to our current understanding on microbial and chemical ecology of seagrasses, implying potential involvement of the seagrass microbiome, especially the leaf epiphytes, in reduction of pathogen load in seawater. Such antibiotic activity is not only beneficial for the health of ocean, human and aquaculture sector, especially in the context of climate change that is expected to exacerbate all infectious diseases, but may also assist seagrass conservation and management strategies.