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Two Members of a Network of Putative Na+/H+ Antiporters Are Involved in Salt and pH Tolerance of the Freshwater Cyanobacterium Synechococcus elongatus

ABSTRACT Synechococcus elongatus strain PCC 7942 is an alkaliphilic cyanobacterium that tolerates a relatively high salt concentration as a freshwater microorganism. Its genome sequence revealed seven genes, nha1 to nha7 (syn_pcc79420811, syn_pcc79421264, syn_pcc7942359, syn_pcc79420546, syn_pcc79420307, syn_pcc79422394, and syn_pcc79422186), and the deduced amino acid sequences encoded by these genes are similar to those of Na+/H+ antiporters. The present work focused on molecular and functional characterization of these nha genes encoding Na+/H+ antiporters. Our results show that of the nha genes expressed in Escherichia coli, only nha3 complemented the deficient Na+/H+ antiporter activity of the Na+-sensitive TO114 recipient strain. Moreover, two of the cyanobacterial strains with separate disruptions in the nha genes (Δnha1, Δnha2, Δnha3, Δnha4, Δnha5, and Δnha7) had a phenotype different from that of the wild type. In particular, ΔnhA3 cells showed a high-salt- and alkaline-pH-sensitive phenotype, while Δnha2 cells showed low salt and alkaline pH sensitivity. Finally, the transcriptional profile of the nha1 to nha7 genes, monitored using the real-time PCR technique, revealed that the nha6 gene is upregulated and the nha1 gene is downregulated under certain environmental conditions.