Leaf Damage Is Associated with Alteration of Microbiome Composition and Abundance in the Spartina alterniflora Phyllosphere

Spartina alterniflora, the dominant plant species in salt marshes along the Atlantic and Gulf of Mexico coastlines of the Americas, is affected by disease and sudden vegetation dieback. Despite the foundational role of S. alterniflora in low-elevation salt marshes, the response of the native leaf-associated microbiome (i.e., phyllosphere microbiome) to leaf damage resulting from disease and environmental stress has not been explored. We hypothesized that healthy and damaged plants would show differentiation in their phyllosphere microbiomes following primary infection or exposure to environmental stressors. Here, we analyzed changes in prokaryotic and fungal relative abundance, diversity, and community composition in the S. alterniflora phyllosphere microbiome. We compared natural marsh and greenhouse plants in Georgia and South Carolina, USA, and collected leaves from healthy and damaged natural plants across two contrasting Spartina phenotypes that differ in their exposure to environmental stress. Our results show that plant origin (i.e., greenhouse vs. natural marsh), plant health status (i.e., healthy vs. damaged), and plant phenotype (i.e., short vs. tall Spartina) affect microbial relative abundance, alpha diversity, and community composition in the S. alterniflora phyllosphere. Damaged leaves presented higher microbial abundance and alpha diversity than healthy leaves, suggesting microbial proliferation following leaf damage. Plants raised from seeds in the greenhouse presented the lowest microbial abundance and Shannon diversity for both prokaryotic and fungal communities, indicating that in natural ecosystems the phyllosphere microbiota is acquired predominantly through horizontal transmission from the environment. Overall, this study provides novel insights into the assembly of the S. alterniflora phyllosphere microbiome.