High and changing salt concentrations represent major abiotic factors limiting the growth of microorganisms. During their long evolution, cyanobacter

Photorespiratory 2-phosphoglycolate (2PG) metabolism is essential for photosynthesis in higher plants but thought to be superfluous in cyanobacteria because of their ability to concentrate CO ₂ internally and thereby inhibit photorespiration. Here, we show that 3 routes for 2PG metabolism are present in the model cyanobacterium Synechocystis sp. strain PCC 6803. In addition to the photorespiratory C2 cycle characterized in plants, this cyanobacterium also possesses the bacterial glycerate pathway and is able to completely decarboxylate glyoxylate via oxalate. A triple mutant with defects in all 3 routes of 2PG metabolism exhibited a high-CO ₂ -requiring (HCR) phenotype. All these catabolic routes start with glyoxylate, which can be synthesized by 2 different forms of glycolate dehydrogenase (GlcD). Mutants defective in one or both GlcD proteins accumulated glycolate under high CO ₂ level and the double mutant Δ glcD1 /Δ glcD2 was unable to grow under low CO ₂ . The HCR phenotype of both the double and the triple mutant could not be attributed to a significantly reduced affinity to CO ₂ , such as in other cyanobacterial HCR mutants defective in the CO ₂ -concentrating mechanism (CCM). These unexpected findings of an HCR phenotype in the presence of an active CCM indicate that 2PG metabolism is essential for the viability of all organisms that perform oxygenic photosynthesis, including cyanobacteria and C3 plants, at ambient CO ₂ conditions. These data and phylogenetic analyses suggest cyanobacteria as the evolutionary origin not only of oxygenic photosynthesis but also of an ancient photorespiratory 2PG metabolism.

In this chapter, we mainly focus on the acclimation of cyanobacteria to the changing ambient CO₂ and discuss mechanisms of inorganic carbon (C_i) uptake, photorespiration, and the regulation among the metabolic fluxes involved in photoautotrophic, photomixotrophic and heterotrophic growth. The structural components for several of the transport and uptake mechanisms are described and the progress towards elucidating their regulation is discussed in the context of studies, which have documented metabolomic changes in response to changes in C_i availability. Genes for several of the transport and uptake mechanisms are regulated by transcriptional regulators that are in the LysR-transcriptional regulator family and are known to act in concert with small molecule effectors, which appear to be well-known metabolites. Signals that trigger changes in gene expression and enzyme activity correspond to specific “regulatory metabolites” whose concentrations depend on the ambient C_i availability. Finally, emerging evidence for an additional layer of regulatory complexity involving small non-coding RNAs is discussed.

The long evolutionary history and photo-autotrophic lifestyle of cyanobacteria has allowed them to colonize almost all photic habitats on Earth, including environments with high or fluctuating salinity. Their basal salt acclimation strategy includes two principal reactions, the active export of ions and the accumulation of compatible solutes. Cyanobacterial salt acclimation has been characterized in much detail using selected model cyanobacteria, but their salt sensing and regulatory mechanisms are less well understood. Here, we briefly review recent advances in the identification of salt acclimation processes and the essential genes/proteins involved in acclimation to high salt. This knowledge is of increasing importance because the necessary mass cultivation of cyanobacteria for future use in biotechnology will be performed in sea water. In addition, cyanobacterial salt resistance genes also can be applied to improve the salt tolerance of salt sensitive organisms, such as crop plants.

Concerted changes in the transcriptional pattern and physiological traits that result from long-term (here defined as up to 24 h) limitation of inorganic carbon (Ci) have been investigated for the cyanobacterium Synechocystis sp. strain PCC 6803. Results from reverse transcription-polymerase chain reaction and genome-wide DNA microarray analyses indicated stable up-regulation of genes for inducible CO2 and HCO3 − uptake systems and of the rfb cluster that encodes enzymes involved in outer cell wall polysaccharide synthesis. Coordinated up-regulation of photosystem I genes was further found and supported by a higher photosystem I content and activity under low Ci (LC) conditions. Bacterial-type glycerate pathway genes were induced by LC conditions, in contrast to the genes for the plant-like photorespiratory C2 cycle. Down-regulation was observed for nitrate assimilation genes and surprisingly also for almost all carboxysomal proteins. However, for the latter the observed elongation of the half-life time of the large subunit of Rubisco protein may render compensation. Mutants defective in glycolate turnover (ΔglcD and ΔgcvT) showed some transcriptional changes under high Ci conditions that are characteristic for LC conditions in wild-type cells, like a modest down-regulation of carboxysomal genes. Properties under LC conditions were comparable to LC wild type, including the strong response of genes encoding inducible high-affinity Ci uptake systems. Electron microscopy revealed a conspicuous increase in number of carboxysomes per cell in mutant ΔglcD already under high Ci conditions. These data indicate that an increased level of photorespiratory intermediates may affect carboxysomal components but does not intervene with the expression of majority of LC inducible genes.