Co-occurring microorganisms regulate the succession of cyanobacterial harmful algal blooms*

Cyanobacterial harmful algal blooms (CyanoHABs) have been found to transmit from N2 fixer-dominated to nonN2 fixer-dominated in many freshwater environments when the supply of N decreases. To elucidate the mechanisms underlying such counter-intuitive CyanoHAB species succession, metatranscriptomes (biotic data) and water quality-related variables (abiotic data) were analyzed weekly during a bloom season in Harsha Lake, a multipurpose lake that serves as a drinking water source and recreational ground. Our results showed that CyanoHABs in Harsha Lake started with N2-fixing Anabaena in June (ANA stage) when N was high, and transitioned to non-N2-fixing Microcystis- and Planktothrix-dominated in July (MIC-PLA stage) when N became limited (low TN/TP). Meanwhile, the concentrations of cyanotoxins, i.e., microcystins were significantly higher in the MIC-PLA stage. Water quality results revealed that N species (i.e., TN, TN/TP) and water temperature were significantly correlated with cyanobacterial biomass. Expression levels of several C- and N-processing-related cyanobacterial genes were highly predictive of the biomass of their species. More importantly, the biomasses of Microcystis and Planktothrix were also significantly associated with expressions of microbial genes (mostly from heterotrophic bacteria) related to processing organic substrates (alkaline phosphatase, peptidase, carbohydrateactive enzymes) and cyanophage genes. Collectively, our results suggest that besides environmental conditions and inherent traits of specific cyanobacterial species, the development and succession of CyanoHABs are regulated by co-occurring microorganisms. Specifically, the co-occurring microorganisms can alleviate the nutrient limitation of cyanobacteria by remineralizing organic compounds.

Automated summary

CyanoHABs in Harsha Lake shifted from N2 fixer-dominated Anabaena to non-N2 fixer-dominated Microcystis and Planktothrix as nitrogen supply decreased. The concentrations of cyanotoxins were significantly higher when nitrogen became limited. Water quality results indicated significant correlations between nitrogen species, water temperature, and cyanobacterial biomass. Additionally, the expression levels of certain C- and N-processing-related cyanobacterial genes were highly predictive of species biomass.