Glycogen Synthesis and Metabolite Overflow Contribute to Energy Balancing in Cyanobacteria

Cano, Mélissa; Holland, Steven C.; Artier, Juliana; Burnap, Rob L.; Ghirardi, Maria L.; Morgan, John A.; Yu, Jianping

doi:10.1016/j.celrep.2018.03.083

Cited by 114 publications

(96 citation statements)

References 30 publications

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“…However, from the perspective of optimal resource allocation, glycogen accumulation is seemingly suboptimal, since the required energy and carbon is stored and not utilized to enhance growth. Various growth limitations are known to induce accumulation of storage products, including glycogen (Monshupanee and Incharoensakdi, 2014), and a recent study showed that glycogen plays an important role in energy balancing and energy homeostasis in Synechocystis (Cano et al, 2018). We therefore hypothesize that the observed increase in glycogen content, in the absence of other stress factors, is consistent with a limitation in standard BG-11 medium.…”

Section: Maximal Growth Rates and Glycogen Accumulationsupporting

confidence: 55%

Quantitative insights into the cyanobacterial cell economy

Zavřel

Faizi

Loureiro

et al. 2018

Preprint

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Phototrophic microorganisms are promising resources for green biotechnology. 13 Compared to heterotrophic microorganisms, however, the cellular economy of phototrophic 14 growth is still insufficiently understood. We provide a quantitative analysis of light-limited, 15 light-saturated, and light-inhibited growth of the cyanobacterium Synechocystis sp. PCC 6803 using 16 a reproducible cultivation setup. We report key physiological parameters, including growth rate, cell 17 size, and photosynthetic activity over a wide range of light intensities. Intracellular proteins were 18 quantified to monitor proteome allocation as a function of growth rate. Among other physiological 19 adaptations, we identify an upregulation of the translational machinery and downregulation of light 20 harvesting components with increasing light intensity and growth rate. The resulting growth laws 21 are discussed in the context of a coarse-grained model of phototrophic growth and available data 22 obtained by a comprehensive literature search. Our insights into quantitative aspects of 23 cyanobacterial adaptations to different growth rates have implications to understand and optimize 24 photosynthetic productivity. 25 26 2014). While quantitative insight into the cellular economy of phototrophic microorganisms is 36 still scarce, the cellular economy of heterotrophic growth has been studied extensively-starting 37 with the seminal works of Monod, Neidhardt, and others (Neidhardt et al., 1990; Neidhardt, 1999; 38 Jun et al., 2018) to more recent quantitative studies of microbial resource allocation (Molenaar 39 et al.40 Maitra and Dill, 2015; Weiße et al., 2015). In response to changing environments, heterotrophic 41 1 of 28 Manuscript submitted to eLife microorganisms are known to differentially allocate their resources: with increasing growth rate, 42 heterotrophic microorganisms typically exhibit upregulation of ribosomes and other proteins 43 related to translation and protein synthesis (Scott et al., 2010; Molenaar et al., 2009; Peebo et al., 44 2015), exhibit complex changes in transcription profiles, e.g. (Klumpp et al., 2009; Matsumoto et al., 45 2013), and increase cell size (Kafri et al., 2016). The molecular limits of heterotrophic growth have 46 been described thoroughly (Kafri et al., 2016; Erickson et al., 2017; Scott et al., 2014; Metzl-Raz 47 et al., 2017; Klumpp et al., 2013). 48 In contrast, only few studies so far have addressed the limits of cyanobacterial growth from an 49 experimental perspective (Bernstein et al., 2016; Yu et al., 2015; Abernathy et al., 2017; Ungerer 50 et al., 2018; Jahn et al., 2018). Of particular interest were the adaptations that enable fast pho-51 toautotrophic growth (Bernstein et al., 2016; Yu et al., 2015; Abernathy et al., 2017; Ungerer et al., 52 2018). The cyanobacterium with the highest known photoautotrophic growth rate, growing with a 53 doubling time of up to ∼ 1.5h, is the strain Synechococcus elongatus UTEX 2973 (Ungerer et al., 54 2018). Compared to its c...

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Section: Maximal Growth Rates and Glycogen Accumulationsupporting

confidence: 55%

Quantitative insights into the cyanobacterial cell economy

Zavřel

Faizi

Loureiro

et al. 2018

Preprint

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“…Glycogen synthase genes, absent in plastids, were possibly among the first genes to be lost and this event may have helped to achieve the early hostÀendosymbiont metabolic integration (Gavelis & Gile, 2018). Glycogen synthase-defective mutant cyanobacteria release organic carbon outside the cell as a homeostatic response to cope with excessive photosynthate production and the inability to store it as glycogen (Cano et al, 2018). Therefore, it is possible that inefficient glycogen storage allowed the leakage of photosynthates that could be used by the host before the evolution of a specific and more efficient photosynthate export system.…”

Section: Arc Ha Ep La S T Id Amentioning

confidence: 99%

Horizontal and endosymbiotic gene transfer in early plastid evolution

2019

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Summary Plastids evolved from a cyanobacterium that was engulfed by a heterotrophic eukaryotic host and became a stable organelle. Some of the resulting eukaryotic algae entered into a number of secondary endosymbioses with diverse eukaryotic hosts. These events had major consequences on the evolution and diversification of life on Earth. Although almost all plastid diversity derives from a single endosymbiotic event, the analysis of nuclear genomes of plastid‐bearing lineages has revealed a mosaic origin of plastid‐related genes. In addition to cyanobacterial genes, plastids recruited for their functioning eukaryotic proteins encoded by the host nucleus and also bacterial proteins of noncyanobacterial origin. Therefore, plastid proteins and plastid‐localised metabolic pathways evolved by tinkering and using gene toolkits from different sources. This mixed heritage seems especially complex in secondary algae containing green plastids, the acquisition of which appears to have been facilitated by many previous acquisitions of red algal genes (the ‘red carpet hypothesis’).

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“…(Cano et al, 2018), there might even be a flux of 12 C to 1,2-propanediol via the glycogen pool, which would not be seen in our experiments. Due to the glycogen synthesis and degradation cycle, which maintains the energy balance in Synechocystis sp.…”

Section: 2-propanediol Is Partly Derived From Glycogenmentioning

confidence: 54%

“…Due to the glycogen synthesis and degradation cycle, which maintains the energy balance in Synechocystis sp. (Cano et al, 2018), there might even be a flux of 12 C to 1,2-propanediol via the glycogen pool, which would not be seen in our experiments.…”

Section: Minimizing 13 Co 2 Consumption For Costefficient Labeling mentioning

confidence: 54%

Cellular physiology controls photoautotrophic production of 1,2‐propanediol from pools of CO₂ and glycogen

David

Schmid

Bühler

2018

Biotech & Bioengineering

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Synechocystis sp. PCC 6803 PG is a cyanobacterial strain capable of synthesizing 1, 2-propanediol from carbon dioxide (CO 2 ) via a heterologous three-step pathway and a methylglyoxal synthase (MGS) originating from Escherichia coli as an initial enzyme.The production window is restricted to the late growth and stationary phase and is apparently coupled to glycogen turnover. To understand the underlying principle of the carbon partitioning between the Calvin-Benson-Bassham (CBB) cycle and glycogen in the context of 1,2-propanediol production, experiments utilizing 13 C labeled CO 2 have been conducted. Carbon fluxes and partitioning between biomass, storage compounds, and product have been monitored under permanent illumination as well as under dark conditions. About one-quarter of the carbon incorporated into 1,2-propanediol originated from glycogen, while the rest was derived from CO 2 fixed in the CBB cycle during product formation. Furthermore, 1,2-propanediol synthesis was depending on the availability of photosynthetic active radiation and glycogen catabolism. We postulate that the regulation of the MGS from E. coli conflicts with the heterologous reactions leading to 1,2-propanediol in Synechocystis sp. PCC 6803 PG.Additionally, homology comparison of the genomic sequence to genes encoding for the methylglyoxal bypass in E. coli suggested the existence of such a pathway also in Synechocystis sp. PCC 6803. These findings are critical for all heterologous pathways coupled to the CBB cycle intermediate dihydroxyacetone phosphate via a MGS and reveal possible engineering targets for rational strain optimization.

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Glycogen Synthesis and Metabolite Overflow Contribute to Energy Balancing in Cyanobacteria

Cited by 114 publications

References 30 publications

Quantitative insights into the cyanobacterial cell economy

Quantitative insights into the cyanobacterial cell economy

Horizontal and endosymbiotic gene transfer in early plastid evolution

Cellular physiology controls photoautotrophic production of 1,2‐propanediol from pools of CO₂ and glycogen

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Glycogen Synthesis and Metabolite Overflow Contribute to Energy Balancing in Cyanobacteria

Cited by 114 publications

References 30 publications

Quantitative insights into the cyanobacterial cell economy

Quantitative insights into the cyanobacterial cell economy

Horizontal and endosymbiotic gene transfer in early plastid evolution

Cellular physiology controls photoautotrophic production of 1,2‐propanediol from pools of CO2 and glycogen

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Product

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Cellular physiology controls photoautotrophic production of 1,2‐propanediol from pools of CO₂ and glycogen