Adjustments to Photosystem Stoichiometry and Electron Transfer Proteins Are Key to the Remarkably Fast Growth of the Cyanobacterium Synechococcus elongatus UTEX 2973

Abstract

At the genome level, Synechococcus elongatus UTEX 2973 (Synechococcus 2973) is nearly identical to the model cyanobacterium Synechococcus elongatus PCC 7942 (Synechococcus 7942) with only 55 single nucleotide differences separating the two strains. Despite the high similarity between the two strains, Synechococcus 2973 grows three times faster, accumulates significantly more glycogen, is tolerant to extremely high light intensities, and displays higher photosynthetic rates. The high homology between the two strains provides a unique opportunity to examine the factors that lead to increased photosynthetic rates. We compared the photophysiology of the two strains and determined the differences in Synechococcus 2973 that lead to increased photosynthetic rates and the concomitant increase in biomass production. In this study, we identified inefficiencies in the electron transport chain of Synechococcus 7942 that have been alleviated in Synechococcus 2973. Photosystem II (PSII) capacity is the same in both strains. However, Synechococcus 2973 exhibits a 1.6-fold increase in PSI content, a 1.5-fold increase in cytochrome b6f content, and a 2.4-fold increase in plastocyanin content on a per cell basis. The increased content of electron carriers allows a higher flux of electrons through the photosynthetic electron transport chain, while the increased PSI content provides more oxidizing power to maintain upstream carriers ready to accept electrons. These changes serve to increase the photosynthetic efficiency of Synechococcus 2973, the fastest growing cyanobacterium known.

Pooled CRISPRi screening of the cyanobacteriumSynechocystissp. PCC 6803 for enhanced growth, tolerance, and chemical production

“…Cyanobacterial NDH-1 complexes participate in cyclic electron flow around PSI, respiratory electron flow, and CO 2 uptake [29][30][31] . An increase in PSI activity at high light can dissipate pressure in the electron transport chain; a similar phenomenon was reported to contribute to high-light tolerance and faster growth in Synechococcus elongatus UTEX 2973 compared to its close relative Synechococcus PCC 7942 32 . Interestingly, the high-light responsive transcription factor RpaB (slr0947, regulator of phycobilisome association B) was also up-regulated in multiple mutants.…”

Quantitative insights into the cyanobacterial cell economy

“…The cyanobacterium with the highest known photoautotrophic growth rate, growing with a doubling time of up to T D ∼ 1.9h, is the strain Synechococcus elongatus UTEX 2973. Compared to its closest relative, Synechococcus elongatus PCC 7942, the strain shows several physiological adaptation, such as higher PSI and cytochrome b 6 f content per cell (Ungerer et al, 2018), lower metabolite pool in central metabolism, less glycogen accumulation, and higher electron charge (Abernathy et al, 2017). Recently, high light was reported to promote the transcription of genes associated with central metabolic pathways, repression of phycobilisome genes, and accelerated glycogen accumulation rates (Tan et al, 2018) While these studies point to strain-specific differences and are important for characterizing non-model microbial metabolism (Abernathy et al, 2017), the general principles of resource allocation in photoautotrophic metabolism and the laws of phototrophic growth are still poorly understood.…”

“…In contrast, only few studies so far have addressed the limits of cyanobacterial growth from an experimental perspective (Bernstein et al, 2016;Yu et al, 2015;Abernathy et al, 2017;Ungerer et al, 2018). Of particular interest were the adaptations that enable fast photoautotrophic growth (Bernstein et al, 2016;Yu et al, 2015;Abernathy et al, 2017;Ungerer et al, 2018). The cyanobacterium with the highest known photoautotrophic growth rate, growing with a doubling time of up to T D ∼ 1.9h, is the strain Synechococcus elongatus UTEX 2973.…”

On the use of oxygenic photosynthesis for the sustainable production of commodity chemicals

“…Therefore, an exciting development is the characterization of Synechococcus elongatus UTEX 2973 (Yu et al ), which appears to have a superior growth rate as compared to many other cyanobacteria. In a recent publication the authors reported its maximal growth rate to be 0.46 h −1 , quoted as a doubling time of 1.5 h (Ungerer et al ). Unfortunately, these latter numbers are a bit ambiguous because the experiment from which they were derived, is described to be performed at 42°C in the text of the paper and at 38°C in the legend of the relevant figure (Fig.…”