The impact of the cyanobacterial carbon-regulator protein SbtB and of the second messengers cAMP and c-di-AMP on CO2-dependent gene expression

The amount of inorganic carbon (C-i) fluctuates in aquatic environments. Cyanobacteria evolved a C-i-concentrating mechanism (CCM) that is regulated at different levels. The regulator SbtB binds to the second messengers cAMP or c-di-AMP and is involved in acclimation to low C-i (LC) in Synechocystis sp. PCC 6803. Here, we investigated the role of SbtB and of associated second messengers at different C-i conditions. The transcriptome of wild-type (WT) Synechocystis and the Delta sbtB mutant were compared with Delta cya1, a mutant defective in cAMP production, and Delta dacA, a mutant defective in generating c-di-AMP. A defined subset of LC-regulated genes in the WT was already changed in Delta sbtB under high C-i (HC) conditions. This response of Delta sbtB correlated with a diminished induction of many CCM-associated genes after LC shift in this mutant. The Delta cya1 mutant showed less deviation from WT, whereas Delta dacA induced CCM-associated genes under HC. Metabolome analysis also revealed differences between the strains, whereby Delta sbtB showed slower accumulation of 2-phosphoglycolate and Delta dacA differences among amino acids compared to WT. Collectively, these results indicate that SbtB regulates a subset of LC acclimation genes while c-di-AMP and especially cAMP appear to have a lesser impact on gene expression under different C-i availabilities.