Submerged macrophytes and their epiphytic microbes form a "holobiont" that plays crucial roles in regulating the biogeochemical cycles of aquatic ecosystems but is sensitive to environmental disturbances such as ammonium loadings. Increasingly more studies suggest that plants may actively seek help from surrounding microbial communities whereby conferring benefits in responding to particular abiotic stresses. However, empirical evidence is scarce regarding how aquatic plants reconstruct their microbiomes as a "cry-for-help" against acute ammonium stress. Here, we investigated the temporal dynamics of the phyllosphere and rhizosphere bacterial communities of Vallisneria natans following ammonium stress and recovery periods. The bacterial community diversity of different plant niches exhibited opposite patterns with ammonium stress, that is, decreasing in the phyllosphere while increasing in the rhizosphere. Furthermore, both phyllosphere and rhizosphere bacterial communities underwent large compositional changes at the end of ammonium stress, significantly enriching of several nitrifiers and denitrifiers. Meanwhile, bacterial legacies wrought by ammonium stress were detected for weeks; some plant growth-promoting and stress-relieving bacteria remained enriched even after stress disappeared. Structural equation model analysis showed that the reshaped bacterial communities in plant niches collectively had a positive effect on maintaining plant biomass. Additionally, we applied an age-prediction model to predict the bacterial community's successional trajectory, and the results revealed a persistent change in bacterial community development under ammonium treatment. Our findings highlight the importance of plant-microbe interactions in mitigating plant stress and fostering a better understanding of the assembly of plant-beneficial microbes under ammonium stress in aquatic ecosystems. IMPORTANCE Increasing anthropogenic input of ammonium is accelerating the decline of submerged macrophytes in aquatic ecosystems. Finding efficient ways to release submerged macrophytes from ammonium stress is crucial to maintain their ecological benefits. Microbial symbioses can alleviate abiotic stress in plants, but harnessing these beneficial interactions requires a detailed understanding of plant microbiome responses to ammonium stress, especially over a continuous time course. Here, we tracked the temporal changes in bacterial communities associated with the phyllosphere and rhizosphere of Vallisneria natans during ammonium stress and recovery periods. Our results showed that severe ammonium stress triggers a plant-driven timely reshaping of the associated bacterial community in a niche-specific strategy. The reassembled bacterial communities could potentially benefit the plant by positively contributing to nitrogen transformation and plant growth promotion. These findings provide empirical evidence regarding the adaptive strategy of aquatic plants whereby they recruit beneficial microbes against ammonium stress.
Keywords: ammonium stress; bacterial community succession; phyllosphere; rhizosphere; submerged macrophyte.