Microcystis-triggered shifts in the symbiotic microbiome of Myriophyllum spicatum rapidly suppress Microcystis aeruginosa

Abstract

While the suppression of toxic cyanobacteria by aquatic plants has long been recognized, few studies have clearly differentiated between the allelopathic effects of the plant itself and the inhibitory influence of its associated microbiome. This study aimed to clarify the primary inhibitory agent by pre-culturing Myriophyllum spicatum (Eurasian watermilfoil) under three conditions: (1) BG11 medium, (2) live Microcystis aeruginosa KW culture, and (3) a Microcystis-symbiotic microbiome (excluding Microcystis cells). After a 7-day pre-culture, Myriophyllum shoots were transferred to fresh Microcystis culture. The Myriophyllum pre-cultured in Microcystis culture exhibited rapid inhibition against Microcystis (84% within day 1), whereas the Myriophyllum pre-cultured in BG11 medium showed delayed responses (89% by day 7). In contrast, inhibition remained below 50% in the Myriophyllum pre-cultured with the Microcystis-symbiotic microbiome. Notably, plant-derived soluble compounds exhibited weak inhibitory effects, whereas the microbiome showed stronger inhibitory activity, indicating that the plant-associated microbiome plays a more dominant role than the plant itself. Exposure to Microcystis triggered significant shifts in plant-symbiotic microbial community composition, leading to rapid enhancement of inhibitory activity in the Myriophyllum microbiome. Microbial community analysis identified 28 bacterial taxa closely associated with the inhibitory response, including strains involved in organic matter degradation, adhesion, biofilm formation, and predatory behavior. Meta-transcriptomic analysis further confirmed increased expression of genes related to bacterial adhesion, biofilm formation, and carbohydrate metabolism following Microcystis exposure, highlighting functional adaptations linked to cyanobacterial suppression. These findings underline the role of microbiome-mediated cyanobactericidal mechanisms, providing new insights into a nature-based solution for mitigating Microcystis-dominated harmful algal blooms.