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.

Widespread Distribution and Adaptive Degradation of Microcystin Degrader (mlr-Genotype) in Lake Taihu, China

Microbial degradation is an important route for removing environmental microcystins (MCs). Here, we investigated the ecological distribution of microcystin degraders (mlr-genotype), and the relationship between the substrate specificity of the microcystin degrader and the profile of microcystin congener production in the habitat. We showed that microcystin degraders were widely distributed and closely associated with Microcystis abundance in Lake Taihu, China. We characterized an indigenous degrader, Sphingopyxis N5 in the northern Lake Taihu, and it metabolized six microcystin congeners in increasing order (RR > LR > YR > LA > LF and LW). Such a substrate-specificity pattern was congruent to the order of the dominance levels of these congeners in northern Lake Taihu. Furthermore, a meta-analysis on global microcystin degraders revealed that the substrate-specificity patterns varied geographically, but generally matched the profiles of microcystin congener production in the degrader habitats, and the indigenous degrader typically metabolized well the dominant MC congeners, but not the rare congeners in the habitat. This highlighted the phenotypic congruence between microcystin production and degradation in natural environments. We theorize that such congruence resulted from the metabolic adaptation of the indigenous degrader to the local microcystin congeners. Under the nutrient microcystin selection, the degraders might have evolved to better exploit the locally dominant congeners. This study provided the novel insight into the ecological distribution and adaptive degradation of microcystin degraders.