Sucrose synthase and RuBisCo expression is similarly regulated by the nitrogen source in the nitrogen-fixing cyanobacterium Anabaena sp.

Curatti, Leonardo; Giarrocco, Laura Estela; Salerno, Graciela L.

doi:10.1007/s00425-005-0142-7

Cited by 32 publications

(66 citation statements)

References 35 publications

(52 reference statements)

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“…was recently demonstrated by Curatti et al (2002), who showed that diazotrophic growth was impaired in a mutant strain overexpressing SuS. Curatti et al (2006) later showed that expression of SuS and Rubisco, a key enzyme in CO 2 fixation during photosynthesis, is similarly downregulated by a N source-dependent developmental program in the heterocysts.…”

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confidence: 88%

“…Suc can either be cleaved by SuS or irreversibly hydrolyzed by two alkaline/neutral invertases (A/N-Inv) when there is high demand for hexoses (Porchia and Salerno, 1996;Cumino et al, 2001Cumino et al, , 2002Curatti et al, 2002;Vargas et al, 2003). Curatti et al (2002Curatti et al ( , 2006 showed SuS to be involved in the cleavage of Suc only in vegetative cells in vivo. Besides, in contrast to a previous report, it has recently been shown that A/N-Invs are also expressed in vegetative cells (Schilling and Ehrnsperger, 1985;Curatti et al, 2002;Vargas et al, 2003).…”

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Carbon Cycling in Anabaena sp. PCC 7120. Sucrose Synthesis in the Heterocysts and Possible Role in Nitrogen Fixation

Cumino¹,

Marcozzi²,

Barreiro³

et al. 2007

Plant Physiol.

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Nitrogen (N) available to plants mostly originates from N 2 fixation carried out by prokaryotes. Certain cyanobacterial species contribute to this energetically expensive process related to carbon (C) metabolism. Several filamentous strains differentiate heterocysts, specialized N 2 -fixing cells. To understand how C and N metabolism are regulated in photodiazotrophically grown organisms, we investigated the role of sucrose (Suc) biosynthesis in N 2 fixation in Anabaena sp. PCC 7120 (also known as Nostoc sp. PCC 7120). The presence of two Suc-phosphate synthases (SPS), SPS-A and SPS-B, directly involved in Suc synthesis with different glucosyl donor specificity, seems to be important in the N 2 -fixing filament. Measurement of enzyme activity and polypeptide levels plus reverse transcription-polymerase chain reaction experiments showed that total SPS expression is greater in cells grown in N 2 versus combined N conditions. Only SPS-B, however, was seen to be active in the heterocyst, as confirmed by analysis of green fluorescent protein reporters. SPS-B gene expression is likely controlled at the transcriptional initiation level, probably in relation to a global N regulator. Metabolic control analysis indicated that the metabolism of glycogen and Suc is likely interconnected in N 2 -fixing filaments. These findings suggest that N 2 fixation may be spatially compatible with Suc synthesis and support the role of the disaccharide as an intermediate in the reduced C flux in heterocystforming cyanobacteria.

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confidence: 88%

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confidence: 99%

Carbon Cycling in Anabaena sp. PCC 7120. Sucrose Synthesis in the Heterocysts and Possible Role in Nitrogen Fixation

Cumino¹,

Marcozzi²,

Barreiro³

et al. 2007

Plant Physiol.

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“…It was first thought that sucrose metabolism was a characteristic of plants, but it was later found in other oxygenic photosynthetic organisms (4,5). In the last decade, Salerno and coworkers demonstrated the importance of sucrose for carbon and nitrogen fixation in filamentous cyanobacteria (6,7). More recently, genomic and phylogenetic analyses revealed the existence of sucrose-related genes in nonphotosynthetic prokaryotes such as proteobacteria, firmicutes, and planctomycetes (4,5,8).…”

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The Crystal Structure of Nitrosomonas europaea Sucrose Synthase Reveals Critical Conformational Changes and Insights into Sucrose Metabolism in Prokaryotes

Diez

Figueroa

et al. 2015

J Bacteriol

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In this paper we report the first crystal structure of a prokaryotic sucrose synthase from the nonphotosynthetic bacterium Nitrosomonas europaea. The obtained structure was in an open form, whereas the only other available structure, from the plant Arabidopsis thaliana, was in a closed conformation. Comparative structural analysis revealed a "hinge-latch" combination, which is critical to transition between the open and closed forms of the enzyme. The N. europaea sucrose synthase shares the same fold as the GT-B family of the retaining glycosyltransferases. In addition, a triad of conserved homologous catalytic residues in the family was shown to be functionally critical in the N. europaea sucrose synthase (Arg567, Lys572, and Glu663). This implies that sucrose synthase shares not only a common origin with the GT-B family but also a similar catalytic mechanism. The enzyme preferred transferring glucose from ADP-glucose rather than UDP-glucose like the eukaryotic counterparts. This predicts that these prokaryotic organisms have a different sucrose metabolic scenario from plants. Nucleotide preference determines where the glucose moiety is targeted after sucrose is degraded. IMPORTANCEWe obtained biochemical and structural evidence of sucrose metabolism in nonphotosynthetic bacteria. Until now, only sucrose synthases from photosynthetic organisms have been characterized. Here, we provide the crystal structure of the sucrose synthase from the chemolithoautotroph N. europaea. The structure supported that the enzyme functions with an open/close induced fit mechanism. The enzyme prefers as the substrate adenine-based nucleotides rather than uridine-based like the eukaryotic counterparts, implying a strong connection between sucrose and glycogen metabolism in these bacteria. Mutagenesis data showed that the catalytic mechanism must be conserved not only in sucrose synthases but also in all other retaining GT-B glycosyltransferases. In plants, sucrose is a major photosynthetic product and plays a key role not only for carbon partition but also in sugar sensing, development, and regulation of gene expression (1-3). It was first thought that sucrose metabolism was a characteristic of plants, but it was later found in other oxygenic photosynthetic organisms (4, 5). In the last decade, Salerno and coworkers demonstrated the importance of sucrose for carbon and nitrogen fixation in filamentous cyanobacteria (6, 7). More recently, genomic and phylogenetic analyses revealed the existence of sucrose-related genes in nonphotosynthetic prokaryotes such as proteobacteria, firmicutes, and planctomycetes (4, 5, 8). It has been suggested that these organisms acquired the genes of sucrose metabolism by horizontal gene transfer (4,5,8). However, analysis of the enzymes encoded by such genes is currently lacking.Nitrosomonas europaea is a chemolithoautotrophic bacterium that obtains energy by oxidizing ammonia to hydroxylamine and nitrite in the presence of oxygen (9). It is a member of the betaproteobacteria group with a putati...

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“…Cyanobacteria exposed to long-term nitrate starvation demonstrate extreme loss of photosynthetic activity and strong bleaching, but the cells remain viable (Sauer et al, 2001). When nitrogen availability changes, cyanobacteria can rebalance the uptake and assimilation of nitrogen (Herrero et al, 2001;Espinosa et al, 2006) and adapt their overall metabolism, including that for carbon fixation and sugar metabolism (Miller et al, 2002;Curatti et al, 2006;Osanai et al, 2006Osanai et al, , 2007.…”

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Concerted Changes in Gene Expression and Cell Physiology of the CyanobacteriumSynechocystissp. Strain PCC 6803 during Transitions between Nitrogen and Light-Limited Growth

et al. 2011

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Physiological adaptation and genome-wide expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to gradual transitions between nitrogen-limited and light-limited growth conditions were measured in continuous cultures. Transitions induced changes in pigment composition, light absorption coefficient, photosynthetic electron transport, and specific growth rate. Physiological changes were accompanied by reproducible changes in the expression of several hundred open reading frames, genes with functions in photosynthesis and respiration, carbon and nitrogen assimilation, protein synthesis, phosphorus metabolism, and overall regulation of cell function and proliferation. Cluster analysis of the nearly 1,600 regulated open reading frames identified eight clusters, each showing a different temporal response during the transitions. Two large clusters mirrored each other. One cluster included genes involved in photosynthesis, which were upregulated during light-limited growth but down-regulated during nitrogen-limited growth. Conversely, genes in the other cluster were down-regulated during light-limited growth but up-regulated during nitrogen-limited growth; this cluster included several genes involved in nitrogen uptake and assimilation. These results demonstrate complementary regulation of gene expression for two major metabolic activities of cyanobacteria. Comparison with batch-culture experiments revealed interesting differences in gene expression between batch and continuous culture and illustrates that continuous-culture experiments can pick up subtle changes in cell physiology and gene expression.

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Sucrose synthase and RuBisCo expression is similarly regulated by the nitrogen source in the nitrogen-fixing cyanobacterium Anabaena sp.

Cited by 32 publications

References 35 publications

Carbon Cycling in Anabaena sp. PCC 7120. Sucrose Synthesis in the Heterocysts and Possible Role in Nitrogen Fixation

Carbon Cycling in Anabaena sp. PCC 7120. Sucrose Synthesis in the Heterocysts and Possible Role in Nitrogen Fixation

The Crystal Structure of Nitrosomonas europaea Sucrose Synthase Reveals Critical Conformational Changes and Insights into Sucrose Metabolism in Prokaryotes

Concerted Changes in Gene Expression and Cell Physiology of the CyanobacteriumSynechocystissp. Strain PCC 6803 during Transitions between Nitrogen and Light-Limited Growth

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