Tasdemir, Deniz , Scarpato, Silvia, Utermann, Caroline , Jensen, Timo, Blümel, Martina , Wenzel-Storjohann, Arlette , Welsch, Claudia and Echelmeyer, Vivien Anne (2024) Epiphytic and endophytic microbiome of the seagrass Zostera marina: Do they contribute to pathogen reduction in seawater?. Science of the Total Environment, 908 . Art.Nr. 168422. DOI 10.1016/j.scitotenv.2023.168422.

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Abstract

Highlights:
• Inhibitory potential of eelgrass microbiome against aquatic and fecal pathogens
• Isolation of epiphytes and endophytes associated with eelgrass leaves and roots
• Particularly leaf epibiotic bacteria exhibit significant antimicrobial activity.
• Rich secondary metabolite composition by untargeted metabolomics
• Potential involvement of eelgrass microbiome in seagrass ecosystem services
Seagrass meadows provide crucial ecosystem services for coastal environments and were shown to reduce the abundance of waterborne pathogens linked to infections in humans and marine organisms in their vicinity. Among potential drivers, seagrass phenolics released into seawater have been linked to pathogen suppression, but the potential involvement of the seagrass microbiome has not been investigated. We hypothesized that the microbiome of the eelgrass Zostera marina, especially the leaf epiphytes that are at direct interface between the seagrass host and the surrounding seawater, inhibit waterborne pathogens thereby contributing to their removal. 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. We assessed the antibiotic activity of microbial extracts against a large panel of common aquatic, human (fecal) and plant pathogens, and mined the metabolome of the most active extracts. The healthy leaf epibiotic bacteria, particularly Streptomyces sp. strain 131, displayed broad-spectrum antibiotic activity superior to some control drugs. Gram-negative bacteria abundant on healthy leaf surfaces, and few endosphere-associated bacteria and fungi also displayed remarkable activities. UPLC-MS/MS-based untargeted metabolomics analyses showed rich specialized metabolite repertoires with low annotation rates, indicating the presence of many undescribed antimicrobials in the extracts. This study contributes to our understanding on microbial and chemical ecology of seagrasses, implying potential involvement of the seagrass microbiome in suppression of pathogens in seawater. Such effect is beneficial for the health of ocean and human, especially in the context of climate change that is expected to exacerbate all infectious diseases. It may also assist future seagrass conservation and management strategies.

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