Cyanobacterial thylakoid membranes represent the active sites for both photosynthetic and respiratory electron transport. We used high-resolution atomic force microscopy to visualise the native organisation and interactions of photosynthetic complexes within the thylakoid membranes from the model cyanobacterium Synechococcus elongatus PCC 7942. The thylakoid membranes are heterogeneous and assemble photosynthetic complexes into functional domains to enhance their coordination and regulation. Under high light, the chlorophyll-binding proteins IsiA are strongly expressed and associates with Photosystem I (PSI) forming highly variable IsiA−PSI supercomplexes to increase the absorption cross-section of PSI. There are also tight interactions of PSI with Photosystem II (PSII), cytochrome b 6 f, ATP synthase, and NAD(P)H dehydrogenase complexes. The organisational variability of these photosynthetic supercomplexes permits efficient linear and cyclic electron transport and bioenergetic regulation. Understanding the organisational landscape and environmental adaptation of cyanobacterial thylakoid membranes may help inform strategies for engineering efficient photosynthetic systems and photo-biofactories.

Oxygenic photosynthesis crucially depends on proteins that possess Fe or Fe/S complexes as co-factors or prosthetic groups. Here, we show that the small regulatory RNA (sRNA) IsaR1 (Iron-Stress-Activated RNA 1) plays a pivotal role in acclimation to low-iron conditions. The IsaR1 regulon consists of more than 15 direct targets, including Fe-containing proteins involved in photosynthetic electron transfer, detoxification of anion radicals, citrate cycle, and tetrapyrrole biogenesis. IsaR1 is essential for maintaining physiological levels of Fe/S cluster biogenesis proteins during iron deprivation. Consequently, IsaR1 affects the acclimation of the photosynthetic apparatus to iron starvation at three levels: (1) directly, via posttranscriptional repression of gene expression; (2) indirectly, via suppression of pigment; and (3) Fe/S cluster biosynthesis. Homologs of IsaR1 are widely conserved throughout the cyanobacterial phylum. We conclude that IsaR1 is a critically important riboregulator. These findings provide a new perspective for understanding the regulation of iron homeostasis in photosynthetic organisms.

The thylakoid membranes of cyanobacteria form a complex intracellular membrane system with a distinctive proteome. The sites of biogenesis of thylakoid proteins remain uncertain, as do the signals that direct thylakoid membrane-integral proteins to the thylakoids rather than to the plasma membrane. Here, we address these questions by using Fluorescent in situ Hybridisation to probe the subcellular location of mRNA molecules encoding core subunits of the photosystems in two cyanobacterial species. These mRNAs cluster at thylakoid surfaces mainly adjacent to the central cytoplasm and the nucleoid, in contrast to mRNAs encoding proteins with other locations. Ribosome association influences the distribution of the photosynthetic mRNAs on the thylakoid surface, but thylakoid affinity is retained in the absence of ribosome association. However, thylakoid association is disrupted in a mutant lacking two mRNA-binding proteins, which likely play roles in targeting photosynthetic proteins to the thylakoid membrane.

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Changing of principal s factor in RNA polymerase holoenzyme to a group 2 s factor redirects transcription when cyanobacteria acclimate to suboptimal environmental conditions. The group 2 sigma factor SigB was found to be important for the growth of the cyanobacterium Synechocystis sp. PCC 6803 in high-salt (0.7 M NaCl) stress but not in mild heat stress at 43°C although the expression of the sigB gene was similarly highly, but only transiently up-regulated at both conditions. The SigB factor was found to regulate many salt acclimation processes. The amount of glucosylglycerol-phosphate synthase, a key enzyme in the production of the compatible solute glucosylglycerol, was lower in the inactivation strain DsigB than in the control strain. Addition of the compatible solute trehalose almost completely restored the growth of the DsigB strain at 0.7 M NaCl. High-salt conditions lowered the chlorophyll and phycobilin contents of the cells while protective carotenoid pigments, especially zeaxanthin and myxoxanthophyll, were up-regulated in the control strain. These carotenoids were up-regulated in the DsigCDE strain (SigB is the only functional group 2 s factor) and down-regulated in the DsigB strain under standard conditions. In addition, the HspA heat shock protein was less abundant and more abundant in the DsigB and DsigCDE strains, respectively, than in the control strain in high-salt conditions. Some cellular responses are common to heat and salt stresses, but pretreatment with mild heat did not protect cells against salt shock although protection against heat shock was evident.