Transcriptome responses to single and combined stressors in seagrass populations from pristine and impacted sites reveal local adaptive features and core stress-response genes

In their natural habitats, seagrasses face multiple abiotic stressors, which can often occur simultaneously. However, most studies have only focused on growth and physiological responses to single stressors. Here, we examined transcriptome responses of the tropical seagrass Halophila stipulacea collected from a northern Gulf of Aqaba pristine site and an anthropogenically-impacted site, grown in a mesocosm, and exposed to ecologically-relevant, single and combined, thermal and excess nutrient stressors. Growth of plants from the impacted site was more tolerant to stress than plants from the pristine site. 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 stress responses. Furthermore, thermal stress exerted a dominant influence upon the transcriptome response to the combined stressor. Transcriptomes of plants from the impacted site displayed reduced responsiveness to stress, the presence of genes exhibiting a “stress-ready” mode of expression under all stressors, 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.