The Small Ca 2+ -Binding Protein CSE Links Ca 2+ Signalling with Nitrogen Metabolism and Filament Integrity in Anabaena Sp. PCC 7120

Background Filamentous cyanobacteria represent model organisms for investigating multicellularity. For many species, nitrogen-fixing heterocysts are formed from photosynthetic vegetative cells under nitrogen limitation. Intracellular Ca 2+ has been implicated in the highly regulated process of heterocyst differentiation but its role remains unclear. Ca 2+ is known to operate more broadly in metabolic signalling in cyanobacteria, although the signalling mechanisms are virtually unknown. A Ca 2+ -binding protein called the Ca 2+ Sensor EF-hand (CSE) is found almost exclusively in filamentous cyanobacteria. Expression of asr1131 encoding the CSE protein in Anabaena sp. PCC 7120 was strongly induced by low CO 2 conditions, and rapidly downregulated during nitrogen step-down. A previous study suggests a role for CSE and Ca 2+ in regulation of photosynthetic activity in response to changes in carbon and nitrogen availability. Results In the current study, a mutant Anabaena sp. PCC 7120 strain lacking asr1131 ( Δcse ) was highly prone to filament fragmentation, leading to a striking phenotype of very short filaments and poor growth under nitrogen-depleted conditions. Transcriptomics analysis under nitrogen-replete conditions revealed that genes involved in heterocyst differentiation and function were downregulated in Δcse , while heterocyst inhibitors were upregulated, compared to the wild-type. Conclusions These results indicate that CSE is required for filament integrity and for proper differentiation and function of heterocysts upon changes in the cellular carbon/nitrogen balance. A role for CSE in transmitting Ca 2+ signals during the first response to changes in metabolic homeostasis is discussed.