Abstract
Classical microbial carbon polymers such as glycogen and polyhydroxybutyrate (PHB) have a crucial impact as both a sink and a reserve under macronutrient stress conditions. Most microbial species exclusively synthesize and degrade either glycogen or PHB. A few bacteria such as the phototrophic model organism Synechocystis sp. PCC 6803 surprisingly produce both physico-chemically different polymers under conditions of high C to N ratios. For the first time, the function and interrelation of both carbon polymers in non-diazotrophic cyanobacteria are analyzed in a comparative physiological study of single- and double-knockout mutants (ΔglgC; ΔphaC; ΔglgC/ΔphaC), respectively. Most of the observed phenotypes are explicitly related to the knockout of glycogen synthesis, highlighting the metabolic, energetic, and structural impact of this process whenever cells switch from an active, photosynthetic ‘protein status’ to a dormant ‘glycogen status’. The carbon flux regulation into glycogen granules is apparently crucial for both phycobilisome degradation and thylakoid layer disassembly in the presence of light. In contrast, PHB synthesis is definitely not involved in this primary acclimation response. Moreover, the very weak interrelations between the two carbon-polymer syntheses indicate that the regulation and role of PHB synthesis in Synechocystis sp. PCC 6803 is different from glycogen synthesis.
Highlights
All microorganisms accumulate carbon biopolymers, namely glycogen and/or poly-βhydroxybutyrate (PHB), which act as cellular sinks as well as stable and yet readily accessible reservoirs for carbon and energy, to acclimate and to cope with starvation conditions, in particular nitrogen starvation leading to high C–to-N ratios of nutrients (Allen, 1984)
To completely abolish carbon-polymer biosynthesis, knockout mutants of either ADP-glucose pyrophosphorylase (AGPase, GlgC) or glycogen synthase (GlgA) for glycogen biosynthesis, or of either β-ketothiolase (PhaA), Acetoacetyl-coenzyme A (CoA) reductase (PhaB), or PHB synthase (PhaC/PhaE) for PHB synthesis were successfully created in different cyanobacterial strains previously (Taroncher-Oldenburg and Stephanopoulos, 2000; Xie et al, 2011; Tsang et al, 2013; van der Woude et al, 2014; Zilliges, 2014)
These substantial changes are tightly related to active glycogen synthesis
Summary
All microorganisms accumulate carbon biopolymers, namely glycogen and/or poly-βhydroxybutyrate (PHB), which act as cellular sinks as well as stable and yet readily accessible reservoirs for carbon and energy, to acclimate and to cope with starvation conditions, in particular nitrogen starvation leading to high C–to-N ratios of nutrients (Allen, 1984). Water-soluble polyglucan composed of 9–13 (1–4)-linked α-D-glucose residues that are interlinked via (1–6)-α-D-glucosidic linkages, forming a highly branched and rigid. The glucose moiety of ADP-glucose is transferred to the non-reducing end of a linear α-(1-4) glucan chain, a reaction catalyzed by glycogen synthase (GlgA). PHB is a non-water-soluble, conformationally amphiphilic, linear, and highly flexible polyester consisting of (R)-3-hydroxybutyrate units, forming 200–500 nm large inclusions (Reusch, 2012; Jendrossek and Pfeiffer, 2014). The first step in PHB synthesis is the condensation of two molecules of acetyl-coenzyme A (CoA) to acetoacetyl-CoA, as catalyzed by β-ketothiolase (PhaA). The subsequent reduction by acetoacetyl-CoA reductase (PhaB) forms the monomeric precursor D-3-hydroxybutyryl-CoA, which is polymerized to PHB by PHB synthase (PhaC/PhaE; Hein et al, 1998). The PHB granule is surrounded by a membraneous surface layer containing phasin protein, which is involved in granule formation and granule attachment to cellular components (Hauf et al, 2015)
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