A Hard Day's Night: Cyanobacteria in Diel Cycles

Abstract

Cyanobacteria are photosynthetic prokaryotes that are influential in global geochemistry and are promising candidates for industrial applications. Because the livelihood of cyanobacteria is directly dependent upon light, a comprehensive understanding of metabolism in these organisms requires taking into account the effects of day-night transitions and circadian regulation. These events synchronize intracellular processes with the solar day. Accordingly, metabolism is controlled and structured differently in cyanobacteria than in heterotrophic bacteria. Thus, the approaches applied to engineering heterotrophic bacteria will need to be revised for the cyanobacterial chassis. Here, we summarize important findings related to diurnal metabolism in cyanobacteria and present open questions in the field.

Keywords: circadian clock; diurnal physiology; light–dark cycles; photosynthesis; redox regulation; signaling nucleotides.

Figure 1.. Shift work: snapshot of cellular activities across the day and night.

A) A representation of an S. elongatus cell with an overview of the major metabolic pathways important for day-night physiology. B) Reactions of glycogen metabolism, TCA pathway, and central metabolism that are present in S. elongatus are provided in more detail. Green arrows in panel B indicate reactions where the respective enzyme has a detectable light/dark-dependent redox modification in Synechocystis sp. PCC 6803 [69]. Data about the peak expression time of circadian genes is indicated using data collected from S. elongatus PCC 7942 [9]. Genes colored in red peak in expression in the subjective morning, genes colored in blue peak in expression in the subjective evening, and genes colored in black have no detectable circadian rhythm in S. elongatus. Essential genes and genes that cause light-dark sensitive phenotypes when mutated are indicated by full yellow and half yellow-half dark grey circles, respectively. Abbreviations: PBS, phycobilisome; PSII, photosystem II; cyt b₆f, cytochrome b₆f; PSI, photosystem I; Fd(red), ferredoxin (reduced); Ru1,5P, ribulose-1,5-bisphosphate; 3PG, 3-phosphoglycerate; 1,3-BPG, 1,3-bisphosphoglycerate; GAP, glyceraldehyde-3-phosphate; F6P, fructose-6-phosphate; G6P, glucose-6-phosphate; G1P, glucose-1-phosphate; 6PGL, 6-phosphogluconolactone; 6PG, 6-phosphogluconate; Ru5P, ribulose-5-phosphate; ac-CoA, acetyl-CoA; aKG, a-ketoglutarate; Glu, glutamate; Gln, glutamine.

Figure 2.. Detoxifying ROS in the diurnal world.

High rates of photosynthetic metabolism in light generate damaging ROS. During the day NADPH produced via photosynthesis can aid in clearing such molecules. At night ROS production ceases, and remaining ROS is cleared by nighttime metabolism. Here, detoxification can be aided by NADPH produced through degradation of glycogen by the OPPP.

Figure 3.. Getting the message: signaling pathways important for the day-night transition.

The signaling pathways effective during the day-to-night transition consist of environmental sensing via RpaB and its cognate histidine protein kinase NblS, circadian status via RpaA, intracellular redox and energy status through changes in concentrations of NADPH and ATP and redox state of the plastoquinone (Pq) pools, chromosome compaction, and nucleotide signaling molecules such as ppGpp and cyclic-di-AMP (synthesized by RelA and CdaA, respectively).