CO2 fixation mediated by the carbon concentrating mechanism enables a rapid response to nitrogen deprivation in cyanobacteria

Cyanobacteria are leading biomass producers of the ocean whose ecological success relies on their ability to respond to dynamic availability of nutrients like CO2 and nitrogen, which require distinct adaptive mechanisms. To survive nitrogen deprivation, cyanobacteria undergo a reversible transition to a dormant mode. Under low CO2 levels, a CO2 concentrating mechanism (CCM) supports their CO2 fixation. While the CCM and nitrogen assimilation have been shown to share some regulatory pathways, how the CCM impacts the response to nitrogen deprivation remains underexplored. In this study, by using mutants of the coastal cyanobacteria Synechococcus sp. PCC 7002 lacking a CCM component, we show that the high rate of carbon fixation mediated by the CCM tunes the speed of the nitrogen deprivation response in {beta}-cyanobacteria. We first show that CCM mutants are deficient in inducing their typical nitrogen deprivation response under atmospheric CO2. However, at higher CO2 concentrations, the CCM mutants induce the nitrogen deprivation response. By combining Rubisco kinetics modeling with measurement of the response speed to nitrogen in various CO2 concentrations, we show that the speed of the nitrogen deprivation response increases linearly with Rubiscos carboxylation rate. We further reveal that the regulation of nitrogen response by the CCM is also present in the distantly related freshwater cyanobacteria Synechococcus elongatus PCC 7942, suggesting a widespread role of this regulation across {beta}-cyanobacteria. This study demonstrates that CO2 fixation by the cyanobacterial CCM is a key regulator of the nitrogen deprivation response, favoring a rapid response to dynamic environments.