Cyanopeptides Restriction and Degradation Co-mediate Microbiota Assembly During a Freshwater Cyanobacterial Harmful Algal Bloom (CyanoHAB)

Cyanobacterial harmful algal blooms (CyanoHABs) are globally intensifying and exacerbated by climate change and eutrophication. However, microbiota assembly mechanisms underlying CyanoHABs remain scenario specific and elusive. Especially, cyanopeptides, as a group of bioactive secondary metabolites of cyanobacteria, could affect microbiota assembly and ecosystem function. Here, the trajectory of cyanopeptides were followed and linked to microbiota during Microcystis-dominated CyanoHABs in lake Taihu, China. The most abundant cyanopeptide classes detected included microginin, spumigin, microcystin, nodularin and cyanopeptolin with total MC-LR-equivalent concentrations between 0.23 and 2051.54 ppb, of which cyanotoxins beyond microcystins (e.g., cyanostatin B and nodularin_R etc.) far exceeded reported organismal IC50 and negatively correlated with microbiota diversity, exerting potential collective eco-toxicities stronger than microcystins alone. The microbial communities were differentiated by size fraction and sampling date throughout CyanoHABs, and surprisingly, their variances were better explained by cyanopeptides (19-38%) than nutrients (0-16%). Cyanopeptides restriction (e.g., inhibition) and degradation are first quantitatively verified as the deterministic drivers governing community assembly, with stochastic processes being mediated by interplay between cyanopeptide dynamics and lake microbiota. This study presents an emerging paradigm in which cyanopeptides restriction and degradation co-mediate lake water microbiota assembly, unveiling new insights about the ecotoxicological significance of CyanoHABs to freshwater ecosystems.