Cyanophage Lysis of the Cyanobacterium Nodularia spumigena Affects the Variability and Fitness of the Host-Associated Microbiome

Abstract

Cyanobacteria are intricately linked with its microbiome through multiple metabolic interactions. We assessed how these interactions might be affected by cyanophage infection and lysis in cyanobacterium Nodularia spumigena. The genome-scale metabolic models and analysis of putative metabolic interactions revealed a bidirectional cross-feeding potential within the N. spumigena microbiome, with heterotrophic bacteria exhibiting a greater level of trophic dependency on the cyanobacterium. Our results indicate that microbes associated with N. spumigena rely on the supply of various amino acids, reduced carbon compounds and protein synthesis cofactors released by the cyanobacterial host. We observed that compositional changes in the N. spumigena microbiome were associated with the multiplicity of infection and increased with increasing initial viral load. Higher mortality of N. spumigena led to decreased variability in the relative abundances of bacteria, suggesting an indirect restriction of their niche space. Lysis of N. spumigena resulted in a substantial decline in the estimated absolute abundances of heterotrophic bacteria, indicating reduced fitness of co-occurring bacteria in the absence of N. spumigena. Altogether, we demonstrate how a gradual increase in viral pressure on the photosynthetic host propagates through the co-occurring microbial community, disrupting cooperative nature and microbial connectivity within the N. spumigena microbiome.