Carbon/Nitrogen Metabolic Balance: Lessons from Cyanobacteria

Zhang, Cheng‐Cai; Zhou, Cong‐Zhao; Burnap, Robert L.; Peng, Ling

doi:10.1016/j.tplants.2018.09.008

Cited by 149 publications

(94 citation statements)

References 87 publications

(182 reference statements)

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“…The gene expression variation between the mutant and the wild type may also be a result of the lowered sulfane sulfur in the mutant, as sulfane sulfur is a known signaling molecule participating in many physiological processes in eukaryotes (58). And from our results, we infer that carbon and sulfur metabolisms can be linked via sulfane sulfur just like carbon and nitrogen metabolisms in cyanobacteria (60,61). As we know, sulfane sulfur can perform as a reductant to help relieve oxidative stress (35,37).…”

Section: Functions Of Sqr In Cyanobacteriamentioning

confidence: 63%

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

Liu

Zhang

Lü

et al. 2020

mBio

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Eutrophication and deoxygenation possibly occur in coastal waters due to excessive nutrients from agricultural and aquacultural activities, leading to sulfide accumulation. Cyanobacteria, as photosynthetic prokaryotes, play significant roles in carbon fixation in the ocean. Although some cyanobacteria can use sulfide as the electron donor for photosynthesis under anaerobic conditions, little is known on how they interact with sulfide under aerobic conditions. In this study, we report that Synechococcus sp. strain PCC7002 (PCC7002), harboring an sqr gene encoding sulfide:quinone oxidoreductase (SQR), oxidized self-produced sulfide to S0, present as persulfide and polysulfide in the cell. The Δsqr mutant contained less cellular S0 and had increased expression of key genes involved in photosynthesis, but it was less competitive than the wild type in cocultures. Further, PCC7002 with SQR and persulfide dioxygenase (PDO) oxidized exogenous sulfide to tolerate high sulfide levels. Thus, SQR offers some benefits to cyanobacteria even under aerobic conditions, explaining the common presence of SQR in cyanobacteria. IMPORTANCE Cyanobacteria are a major force for primary production via oxygenic photosynthesis in the ocean. A marine cyanobacterium, PCC7002, is actively involved in sulfide metabolism. It uses SQR to detoxify exogenous sulfide, enabling it to survive better than its Δsqr mutant in sulfide-rich environments. PCC7002 also uses SQR to oxidize endogenously generated sulfide to S0, which is required for the proper expression of key genes involved in photosynthesis. Thus, SQR has at least two physiological functions in PCC7002. The observation provides a new perspective for the interplays of C and S cycles.

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Section: Functions Of Sqr In Cyanobacteriamentioning

confidence: 63%

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

Liu

Zhang

Lü

et al. 2020

mBio

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“…It has been demonstrated that cyAbrB2 of Synechocystis functions in concert with a global nitrogen regulator, NtcA (17), whose activity is regulated by 2-oxoglutarate (5-9), and the inorganic carbon regulators CmpR and NdhR (21,23). Nitrogen sources (ammonium or nitrate) and/or the CO 2 concentration should affect the 2-oxoglutarate concentration (57) and NtcA activity. However, irrespective of nitrogen sources and CO 2 concentrations, hetP and hepA were similarly induced by calA/cyabrB1 knockdown (Fig.…”

Section: Repression Of Heterocyst Formation In Ammonium Mediummentioning

confidence: 99%

cyAbrB Transcriptional Regulators as Safety Devices To Inhibit Heterocyst Differentiation in Anabaena sp. Strain PCC 7120

et al. 2019

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Cyanobacteria are monophyletic organisms that perform oxygenic photosynthesis. While they exhibit great diversity, they have a common set of genes. However, the essentiality of them for viability has hampered the elucidation of their functions. One example of these genes is cyabrB1 (also known as calA in Anabaena sp. strain PCC 7120), encoding a transcriptional regulator. In the present study, we investigated the function of calA/cyabrB1 in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120 through CRISPR interference, a method that we recently utilized for the photosynthetic production of a useful chemical in this strain. Conditional knockdown of calA/cyabrB1 in the presence of nitrate resulted in the formation of heterocysts. Two genes, hetP and hepA, which are required for heterocyst formation, were upregulated by calA/cyabrB1 knockdown in the presence of combined nitrogen sources. These genes are known to be induced by HetR, a master regulator of heterocyst formation. hetR was not induced by calA/cyabrB1 knockdown. hetP and hepA were repressed by direct binding of CalA/cyAbrB1 to their promoter regions in a HetR-independent manner. In addition, the overexpression of calA/cyabrB1 abolished heterocyst formation upon nitrogen depletion. Also, knockout of calB/cyabrB2 (a paralogue gene of calA/cyabrB1), in addition to knockdown of calA/cyabrB1, enhanced heterocyst formation in the presence of nitrate, suggesting functional redundancy of cyAbrB proteins. We propose that a balance between amounts of HetR and CalA/cyAbrB1 is a key factor influencing heterocyst differentiation during nitrogen stepdown. We concluded that cyAbrB proteins are essential safety devices that inhibit heterocyst differentiation. IMPORTANCE Spore formation in Bacillus subtilis and Streptomyces has been extensively studied as models of prokaryotic nonterminal cell differentiation. In these organisms, many cells/hyphae differentiate simultaneously, which is governed by a network in which one regulator stands at the top. Differentiation of heterocysts in Anabaena sp. strain PCC 7120 is unique because it is terminal, and only 5 to 10% of vegetative cells differentiate into heterocysts. In this study, we identified CalA/cyAbrB1 as a repressor of two genes that are essential for heterocyst formation independently of HetR, a master activator for heterocyst differentiation. This finding is reasonable for unique cell differentiation of Anabaena because CalA/cyAbrB1 could suppress heterocyst differentiation tightly in vegetative cells, while only cells in which HetR is overexpressed could differentiate into heterocysts.

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“…We can conclude, therefore, that 2‐OG is the key element in the connection between oxidative stress and N metabolism. Several studies revealed that 2‐OG is a master regulator metabolite in different organisms, including bacteria, plants and humans (Huergo & Dixon, ; Zhang et al ., ). In this sense, our work highlights a new function of this signalling molecule in cyanobacteria.…”

Section: Discussionmentioning

confidence: 97%

Redox interference in nitrogen status via oxidative stress is mediated by 2‐oxoglutarate in cyanobacteria

2019

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Summary Reactive oxygen species (ROS) are generated naturally in photosynthetic organisms by respiration and photosynthesis. Therefore, detoxification of these compounds, avoiding oxidative stress, is essential for proper cell function. In cyanobacteria, some observations point to a crosstalk between ROS homeostasis, in particular hydrogen peroxide, and nitrogen metabolism by a mechanism independent of known redox regulators. Using glutamine synthetase (GS), a finely regulated enzyme essential for nitrogen assimilation, as a tool, we were able to monitor nitrogen metabolism in relation to oxidative stress. We show that hydrogen peroxide clearly alters the expression of different genes related to nitrogen metabolism, both in the wild‐type strain of the cyanobacterium Synechocystis sp. PCC 6803 and in a mutant strain lacking the catalase‐peroxidase encoded by the katG gene and therefore highly sensitive to oxidative stress. As cyanobacteria perceive nitrogen status by sensing intracellular 2‐oxoglutarate (2‐OG) concentrations, the hydrogen peroxide effect was analysed under different nitrogen conditions in the wild‐type, the ∆katG strain and in a strain able to transport 2‐OG. The results obtained demonstrate that hydrogen peroxide interferes with signalling of cellular carbon : nitrogen status by decreasing the intracellular concentrations of 2‐OG and hence altering the function of the 2‐OG‐sensing global nitrogen regulator NtcA.

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Carbon/Nitrogen Metabolic Balance: Lessons from Cyanobacteria

Cited by 149 publications

References 87 publications

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

cyAbrB Transcriptional Regulators as Safety Devices To Inhibit Heterocyst Differentiation in Anabaena sp. Strain PCC 7120

Redox interference in nitrogen status via oxidative stress is mediated by 2‐oxoglutarate in cyanobacteria

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