Transcriptome responses of two Halophila stipulacea seagrass populations from pristine and impacted habitats, to single and combined thermal and excess nutrient stressors, reveal local adaptive features and core stress-response genes

Abstract

In their natural habitats, seagrasses face multiple abiotic stressors, which can often occur simultaneously. However, most studies investigating the effects of environmental stressors on seagrasses have focused on growth and physiological responses to single stressors. Here, we examined the transcriptome responses of the tropical seagrass Halophila stipulacea collected from a northern Gulf of Aqaba pristine site (South Beach - SB) and an anthropogenically-impacted site (Tur Yam - TY), grown in a mesocosm, and exposed to ecologically-relevant, single and combined, thermal and excess nutrient stressors. The combined thermal and nutrient stressor elicited greater transcriptome reprogramming than the single stressors in both populations and induced the expression of a combination-specific set of genes involved in abiotic and biotic stress responses. Furthermore, thermal stress exerted a more dominant influence than excess nutrient stress upon the transcriptome response to the combined stress. Transcriptomes of plants from the impacted TY site displayed reduced plasticity, the presence of genes exhibiting a "stress-ready" mode of expression under all stresses, and increased resilience (recovery to control transcriptomes). We also identified core stress-response genes that could be leveraged as early indicators of stress in the field. Overall, our data suggest that environmental conditions in seagrass habitats can drive local molecular adaptation, and that the response of seagrasses to combined stressors associated with climate change and coastal anthropogenic stressors cannot be predicted from the response to single stressors.