The tradeoff between resistance to phages and nitrogen fixation in bloom-forming cyanobacteria

Cyanobacterial blooms negatively impact aquatic environments worldwide. Diazotrophic cyanobacteria, such as Cylindrospermopsis, can even form blooms under nitrogen starvation, due to their ability to fix atmospheric nitrogen (N₂). Phages could potentially control cyanobacterial growth; however, cyanobacteria are able to adapt to the presence of phages quite rapidly by acquiring resistance to the phage, thus, the role of phages in bloom dynamics is still unclear. We examined the resistance to phages of two strains of diazotrophic cyanobacteria: the invasive bloom-forming C. raciborskii, and the model strain Nostoc PCC 7120. Our results demonstrate that this resistance, comes with reduced ability to induce heterocyst cells, in which N₂ is fixed. This reduction causes reduced N₂ fixation by the mutant strains, along with reduced growth or even death under nitrogen starvation. Such cost can prevent the survival of phage-resistant cyanobacteria under nitrogen starvation, and may suggest that spontaneous resistance to phages is a transient trait in diazotrophic bloom-forming cyanobacteria. Whole genome sequence analysis of the resistant strains revels new genes essential for heterocyst development and function, and suggests a possible explanation to this intriguing pleiotropy.