Cyanophage lysis reshapes nitrogen cycling and microbiome composition in diazotrophic cyanobacterium Aphanizomenon flos-aquae.

Although it is presumed that viruses play a significant role in nutrient cycling and bacterial community dynamics, this has only rarely been addressed in studies of diazotrophic cyanobacteria. In this study, we therefore examined how cyanophage infection affects the expression of nitrogen (N) cycling genes, N₂ fixation rates, and population structure in the diazotrophic cyanobacterium Aphanizomenon flos-aquae, a prevalent bloom-forming species in temperate brackish and freshwater ecosystems. We also assessed the influence of A. flos-aquae lysis on co-occurring bacterial assemblages throughout an incubation experiment. We found that nitrogen fixation, its release, and the relative availability of different nitrogen forms (e.g. ammonium versus nitrate/nitrite) varied substantially during cyanophage infection, population lysis, and recovery phases. Interestingly, resistant A. flos-aquae subpopulation emerged during viral infection, showed increased expression of N fixation (e.g. nitrogenase (nifH) and heterocyst differentiation regulator (hetR)) and assimilation (e.g. glutamine (glnA) and glutamate (gltB) synthase) genes, as well as higher cell-specific N₂ fixation rates. These changes were accompanied by a fast recovery of A. flos-aquae population structure (e.g. filament length and heterocyte-to-vegetative cell ratio) to pre-infection level, indicating A. flos-aquae ability to quickly compensate for short-term population decline. Lysis of the cyanobacterial host significantly altered the successional trajectory and increased diversification of the co-occurring bacterial community. The compositional changes corresponded well with the prevalent inorganic nitrogen form, implying a substantial, nitrogen-driven reorganization of the microbial network and its interactions within the A. flos-aquae microbiome. This study improves our understanding of nitrogen cycling and microbial dynamics within cyanobacteria-driven communities disturbed by viral infections and lysis.