Blue light induces major changes in the gene expression profile of the cyanobacterium Synechocystis sp. PCC 6803.

Veerle M Luimstra,Klaas J Hellingwerf,J Merijn Schuurmans,Hans C P Matthijs,Jef Huisman

doi:10.1111/ppl.13086

Abstract

Although cyanobacteria absorb blue light, they use it less efficiently for photosynthesis than other colors absorbed by their photosynthetic pigments. A plausible explanation for this enigmatic phenomenon is that blue light is not absorbed by phycobilisomes and, hence, causes an excitation shortage at photosystem II (PSII). This hypothesis is supported by recent physiological studies, but a comprehensive understanding of the underlying changes in gene expression is still lacking. In this study, we investigate how a switch from artificial white light to blue, orange or red light affects the transcriptome of the cyanobacterium Synechocystis sp. PCC 6803. In total, 145 genes were significantly regulated in response to blue light, whereas only a few genes responded to orange and red light. In particular, genes encoding the D1 and D2 proteins of PSII, the PSII chlorophyll‐binding protein CP47 and genes involved in PSII repair were upregulated in blue light, whereas none of the photosystem I (PSI) genes responded to blue light. These changes were accompanied by a decreasing PSI:PSII ratio. Furthermore, many genes involved in gene transcription and translation and several ATP synthase genes were transiently downregulated, concurrent with a temporarily decreased growth rate in blue light. After 6–7 days, when cell densities had strongly declined, the growth rate recovered and the expression of these growth‐related genes returned to initial levels. Hence, blue light induces major changes in the transcriptome of cyanobacteria, in an attempt to increase the photosynthetic activity of PSII and cope with the adverse growth conditions imposed by blue light.

Highlights

Cyanobacteria play a key role in aquatic ecosystems and are widely hailed as the evolutionary ancestors of chloroplasts and are often used as model organisms to study oxygenic photosynthesis
Cell counts and biomass decreased by ~85% and a new steady-state was reached after ~168 h, with 5.2 Æ 1.5 million cells ml−1 (Fig. 1A) and a total biomass of 33.5 Æ 8.0 mm3 l−1 (Fig. 1B)
Blue light at wavelengths ≤450 nm is not absorbed by the PBS (Tandeau de Marsac 2003, Six et al 2007), which usually transfer most of their absorbed light energy to photosystem II (PSII)

Summary

Introduction

Cyanobacteria play a key role in aquatic ecosystems and are widely hailed as the evolutionary ancestors of chloroplasts and are often used as model organisms to study oxygenic photosynthesis. Abbreviations – ATP, adenosine triphosphate; Chl a, chlorophyll a; Hik, histidine kinase; LED, light-emitting diode; NADPH, reduced nicotinamide adenine dinucleotide phosphate; PBS, phycobilisomes; PC, phycocyanin; PSI, photosystem I; PSII, photosystem II. As a consequence, PBScontaining cyanobacteria can be strong competitors in cyan, green or orange light absorbed by their PBS, but they are very poor competitors in blue light ≤450 nm in comparison to photosynthetic organisms with chlorophyll-based lightharvesting complexes (Luimstra et al 2020). Prochlorococcus lacks PBS but instead uses divinylchlorophyll-based light-harvesting complexes quite similar to green algae and terrestrial plants, and it performs very well in blue light as it is the most abundant cyanobacterium in the blue waters of the open ocean (Chisholm et al 1988, Flombaum et al 2013)

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Conclusion