Structure-Function Covariation of Phycospheric Microorganisms Associated with the Typical Cross-Regional Harmful Macroalgal Bloom

Harmful macroalgal blooms represented by green tides have become a worldwide marine ecological problem. Unraveling the structure-function variation of phycospheric microorganisms and their ecological correlation with HMBs is challenging. This issue is still unclear in the natural dynamics of HMBs. ABSTRACT Unravelling the structure-function variation of phycospheric microorganisms and its ecological correlation with harmful macroalgal blooms (HMBs) is a challenging research topic that remains unclear in the natural dynamic process of HMBs. During the world’s largest green tide bloom, causative macroalgae Ulva prolifera experienced dramatic changes in growth state and environmental conditions, providing ideal scenarios for this investment. Here, we assess the phycospheric physicochemical characteristics, the algal host’s biology, the phycospheric bacterial constitutive patterns, and the functional potential during the U. prolifera green tide. Our results indicated that (i) variation in the phycosphere nutrient structure was closely related to the growth state of U. prolifera; (ii) stochastic processes govern phycospheric bacterial assembly, and the contribution of deterministic processes to assembly varied among phycospheric seawater bacteria and epiphytic bacteria; (iii) phycospheric seawater bacteria and epiphytic bacteria exhibited significant heterogeneity variation patterns in community composition, structure, and metabolic potential; and (iv) phycospheric bacteria with carbon or nitrogen metabolic functions potentially influenced the nutrient utilization of U. prolifera. Furthermore, the keystone genera play a decisive role in the structure-function covariation of phycospheric bacterial communities. Our study reveals complex interactions and linkages among environment-algae-bacterial communities which existed in the macroalgal phycosphere and highlights the fact that phycospheric microorganisms are closely related to the fate of the HMBs represented by the green tide. IMPORTANCE Harmful macroalgal blooms represented by green tides have become a worldwide marine ecological problem. Unraveling the structure-function variation of phycospheric microorganisms and their ecological correlation with HMBs is challenging. This issue is still unclear in the natural dynamics of HMBs. Here, we revealed the complex interactions and linkages among environment-algae-bacterial communities in the phycosphere of the green macroalgae Ulva prolifera, which causes the world’s largest green tides. Our study provides new ideas to increase our understanding of the variation patterns of macroalgal phycospheric bacterial communities and the formation mechanisms and ecological effects of green tides and highlights the importance of phycospheric microorganisms as a robust tool to help understand the fate of HMBs.