Functional insights into succession in a phyllospheric microbial community across a full period of aquatic plant litter decomposition

Phyllosphere microbes are essential in the mediation of plant–soil biogeochemical recycling during the decomposition of plant litter in wetland ecosystems. However, there are few studies into microbial community succession in phyllosphere microbial communities in wetlands, and their functional attributes across a full period of wetland plant litter decomposition remain unclear. Here, we collected leaf samples of Typha latifolia var. orientalis (C. Presl.) Rohrb., an emergent wetland plant, during various stages of decomposition (growing, standing, lodging, and submerging stages) to investigate fungal and bacterial assemblage succession in the phyllosphere. We then parsed these assemblages into specific fungal trophic modes and bacterial phenotypes. Over the litter decomposition period, both fungal and bacterial assemblages underwent distinct succession, with generally increasing alpha diversity, and the proportion of litter microbes originating from sediments increased with decomposition. Saprotrophic and pathotrophic fungi dominated the fungal assemblage in the early stages of decomposition, but their dominance was replaced by undefined fungi as decomposition progressed. Relative abundances of both pathotrophic fungi and potentially pathogenic bacteria increased from the growing to the standing stage, implying that there was a turning point in assemblage composition shortly after plant leaf death. Gram-positive and gram-negative bacteria had opposite trends in their relative abundances over successive decomposition stages. When plant litter entered the water, bacteria tolerant of oxidative stress gradually decreased in abundance, but anaerobic bacteria abundance increased. We also aimed to determine the relationships between predicted microbial functional traits and leaf litter physicochemical attributes. Lignin and N content were the predominant predictors of decomposer fungal trophic modes and bacterial phenotypes. These findings provide evidence that the complex litter decomposition seen in wetlands is accompanied by a dynamic cross-kingdom succession of phyllospheric microbial communities, coupled with distinct changes in the phenotypes of the microbes present. Insights into phyllospheric microbial functional traits have implications for better elucidating the plant litter cycle for wetland plants.