Lethality caused by ADP-glucose accumulation is suppressed by salt-induced carbon flux redirection in cyanobacteria.

Francisco J Florencio,Miguel Roldán,Manuel J Mallén-Ponce,Sandra Díaz-Troya,Pablo Ortega-Martínez,Howard Griffiths

doi:10.1093/jxb/erz559

Abstract

Cyanobacteria are widely distributed photosynthetic organisms. During the day they store carbon, mainly as glycogen, to provide the energy and carbon source they require for maintenance during the night. Here, we generate a mutant strain of the freshwater cyanobacterium Synechocystis sp. PCC 6803 lacking both glycogen synthases. This mutant has a lethal phenotype due to massive accumulation of ADP-glucose, the substrate of glycogen synthases. This accumulation leads to alterations in its photosynthetic capacity and a dramatic decrease in the adenylate energy charge of the cell to values as low as 0.1. Lack of ADP-glucose pyrophosphorylase, the enzyme responsible for ADP-glucose synthesis, or reintroduction of any of the glycogen synthases abolishes the lethal phenotype. Viability of the glycogen synthase mutant is also fully recovered in NaCl-supplemented medium, which redirects the surplus of ADP-glucose to synthesize the osmolite glucosylglycerol. This alternative metabolic sink also suppresses phenotypes associated with the defective response to nitrogen deprivation characteristic of glycogen-less mutants, restoring the capacity to degrade phycobiliproteins. Thus, our system is an excellent example of how inadequate management of the adenine nucleotide pools results in a lethal phenotype, and the influence of metabolic carbon flux in cell viability and fitness.

Highlights

Cyanobacteria are prokaryotic organisms that are widely distributed among almost every habitat on Earth.They are especially important in aquatic ecosystems as primary producers and N2 fixers, introducing carbon and nitrogen into the trophic chains
Viability of the glycogen synthase mutant is fully recovered in NaCl-supplemented medium, which redirects the surplus of ADP-glucose to synthesize the osmolite glucosylglycerol
K1, ΔglgA2::SpΩ); Table 1, Supplementary Fig. S1) was viable (Fig. 2A).This finding suggests that the lack of both GlgA1 and GlgA2 in combination with the presence of ADP-glucose pyrophosphorylase (AGP) generates alterations additional to those caused by the lack of glycogen polymer

Summary

Introduction

Cyanobacteria are prokaryotic organisms that are widely distributed among almost every habitat on Earth.They are especially important in aquatic ecosystems as primary producers and N2 fixers, introducing carbon and nitrogen into the trophic chains These organisms had a crucial role in the history of the planet: oxygenic photosynthesis, which releases O2 as a by-product, evolved in ancient cyanobacteria and played a key role in the transition from the primitive anaerobic and reducing atmosphere to the aerobic and oxidizing environment that exists today (Lyons et al., 2014; Soo et al, 2017).A cyanobacterial ancestor gave rise to the plastids in modern photosynthetic eukaryotes by an endosymbiotic process (Ponce-Toledo et al, 2017). Prolonged nitrogen deficiency results in the cells entering a dormant-like state in which they can survive for extended periods of time (Forchhammer and Schwarz, 2019)

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Conclusion