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Sucrose in cyanobacteria: from a salt-response molecule to play a key role in nitrogen fixation.

Kolman MA, Nishi CN, Perez-Cenci M, Salerno GL - Life (Basel) (2015)

Bottom Line: In those prokaryotes, sucrose accumulation has been associated with salt acclimation, and considered as a compatible solute in low-salt tolerant strains.In the last years, functional characterizations of sucrose metabolizing enzymes, metabolic control analysis, cellular localization of gene expressions, and reverse genetic experiments have revealed that sucrose metabolism is crucial in the diazotrophic growth of heterocystic strains, and besides, that it can be connected to glycogen synthesis.This article briefly summarizes the current state of knowledge of sucrose physiological functions in modern cyanobacteria and how they might have evolved taking into account the phylogenetic analyses of sucrose enzymes.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Investigaciones en Biodiversidad y Biotecnología (INBIOTEC-CONICET) and Fundación para Investigaciones Biológicas Aplicadas (FIBA), Mar del Plata B7600DHN, Argentina. mkolman@fiba.org.ar.

ABSTRACT
In the biosphere, sucrose is mainly synthesized in oxygenic photosynthetic organisms, such as cyanobacteria, green algae and land plants, as part of the carbon dioxide assimilation pathway. Even though its central position in the functional biology of plants is well documented, much less is known about the role of sucrose in cyanobacteria. In those prokaryotes, sucrose accumulation has been associated with salt acclimation, and considered as a compatible solute in low-salt tolerant strains. In the last years, functional characterizations of sucrose metabolizing enzymes, metabolic control analysis, cellular localization of gene expressions, and reverse genetic experiments have revealed that sucrose metabolism is crucial in the diazotrophic growth of heterocystic strains, and besides, that it can be connected to glycogen synthesis. This article briefly summarizes the current state of knowledge of sucrose physiological functions in modern cyanobacteria and how they might have evolved taking into account the phylogenetic analyses of sucrose enzymes.

No MeSH data available.


Schematic representation of sucrose metabolism in cyanobacteria. Sucrose biosynthesis involves the sequential action of SPS and SPP, yielding free sucrose and inorganic phosphate. Cyanobacterial SPSs preferentially use ADP-glucose or UDP-glucose, as substrates. The disaccharide degradation can be carried out by the activities of the three different enzymes: (i) SuS that catalyzes a readily reversible reaction but that in vivo acts in the cleavage of sucrose, supplying ADP-glucose, a precursor for glycogen synthesis; however in vitro, SuS can also accept other sugar nucleotides (i.e., UDP) as substrate; (ii) A/N-Inv that irreversible hydrolyzes sucrose into glucose and fructose; and (iii) AMS that is able to catalyze not only sucrose hydrolysis to hexoses, but also to transfer the glucose moiety to a soluble maltooligosaccharide or to an insoluble α 1,4-glucan.
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life-05-00102-f001: Schematic representation of sucrose metabolism in cyanobacteria. Sucrose biosynthesis involves the sequential action of SPS and SPP, yielding free sucrose and inorganic phosphate. Cyanobacterial SPSs preferentially use ADP-glucose or UDP-glucose, as substrates. The disaccharide degradation can be carried out by the activities of the three different enzymes: (i) SuS that catalyzes a readily reversible reaction but that in vivo acts in the cleavage of sucrose, supplying ADP-glucose, a precursor for glycogen synthesis; however in vitro, SuS can also accept other sugar nucleotides (i.e., UDP) as substrate; (ii) A/N-Inv that irreversible hydrolyzes sucrose into glucose and fructose; and (iii) AMS that is able to catalyze not only sucrose hydrolysis to hexoses, but also to transfer the glucose moiety to a soluble maltooligosaccharide or to an insoluble α 1,4-glucan.

Mentions: The identification and functional characterization of sucrose-synthesis related enzymes was first described in Anabaena sp. PCC 7119, a filamentous heterocyst-forming strain [15]. Further studies were carried out in other model cyanobacteria, including Synechocystis sp. PCC 6803 (a freshwater unicellular strain) [16,17], Anabaena sp. PCC 7120 [18,19], Synechococcus sp. PCC 7002 (unicellular marine strain) [10], Microcystis aeruginosa PCC 7806 (a bloom-forming strain) [11], and Synechococcus elongatus PCC 7942 [12]. Basically, for sucrose-biosynthesis, it was shown a similar route to that of plants involving the sequential action of sucrose-phosphate synthase (SPS, U/ADP-glucose: d-fructose-6-phosphate 2-α-d-glucosyltransferase, EC 2.4.1.14) and sucrose-phosphate phosphatase (SPP, sucrose-6F-phosphate-phosphohydrolase, EC 3.1.3.24), yielding free sucrose and Pi (Figure 1). Cyanobacterial SPSs display important biochemical differences in comparison with the orthologous plant proteins. Thus, SPSs are not specific for UDP–glucose and most SPSs can accept ADP–glucose and, to a minor extent, other sugar nucleotides as substrates [15,16,19]. The hydrolysis of the intermediate by SPP leads to an essentially irreversible pathway providing an efficient production of sucrose even at low substrate concentrations [9,13].


Sucrose in cyanobacteria: from a salt-response molecule to play a key role in nitrogen fixation.

Kolman MA, Nishi CN, Perez-Cenci M, Salerno GL - Life (Basel) (2015)

Schematic representation of sucrose metabolism in cyanobacteria. Sucrose biosynthesis involves the sequential action of SPS and SPP, yielding free sucrose and inorganic phosphate. Cyanobacterial SPSs preferentially use ADP-glucose or UDP-glucose, as substrates. The disaccharide degradation can be carried out by the activities of the three different enzymes: (i) SuS that catalyzes a readily reversible reaction but that in vivo acts in the cleavage of sucrose, supplying ADP-glucose, a precursor for glycogen synthesis; however in vitro, SuS can also accept other sugar nucleotides (i.e., UDP) as substrate; (ii) A/N-Inv that irreversible hydrolyzes sucrose into glucose and fructose; and (iii) AMS that is able to catalyze not only sucrose hydrolysis to hexoses, but also to transfer the glucose moiety to a soluble maltooligosaccharide or to an insoluble α 1,4-glucan.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4390843&req=5

life-05-00102-f001: Schematic representation of sucrose metabolism in cyanobacteria. Sucrose biosynthesis involves the sequential action of SPS and SPP, yielding free sucrose and inorganic phosphate. Cyanobacterial SPSs preferentially use ADP-glucose or UDP-glucose, as substrates. The disaccharide degradation can be carried out by the activities of the three different enzymes: (i) SuS that catalyzes a readily reversible reaction but that in vivo acts in the cleavage of sucrose, supplying ADP-glucose, a precursor for glycogen synthesis; however in vitro, SuS can also accept other sugar nucleotides (i.e., UDP) as substrate; (ii) A/N-Inv that irreversible hydrolyzes sucrose into glucose and fructose; and (iii) AMS that is able to catalyze not only sucrose hydrolysis to hexoses, but also to transfer the glucose moiety to a soluble maltooligosaccharide or to an insoluble α 1,4-glucan.
Mentions: The identification and functional characterization of sucrose-synthesis related enzymes was first described in Anabaena sp. PCC 7119, a filamentous heterocyst-forming strain [15]. Further studies were carried out in other model cyanobacteria, including Synechocystis sp. PCC 6803 (a freshwater unicellular strain) [16,17], Anabaena sp. PCC 7120 [18,19], Synechococcus sp. PCC 7002 (unicellular marine strain) [10], Microcystis aeruginosa PCC 7806 (a bloom-forming strain) [11], and Synechococcus elongatus PCC 7942 [12]. Basically, for sucrose-biosynthesis, it was shown a similar route to that of plants involving the sequential action of sucrose-phosphate synthase (SPS, U/ADP-glucose: d-fructose-6-phosphate 2-α-d-glucosyltransferase, EC 2.4.1.14) and sucrose-phosphate phosphatase (SPP, sucrose-6F-phosphate-phosphohydrolase, EC 3.1.3.24), yielding free sucrose and Pi (Figure 1). Cyanobacterial SPSs display important biochemical differences in comparison with the orthologous plant proteins. Thus, SPSs are not specific for UDP–glucose and most SPSs can accept ADP–glucose and, to a minor extent, other sugar nucleotides as substrates [15,16,19]. The hydrolysis of the intermediate by SPP leads to an essentially irreversible pathway providing an efficient production of sucrose even at low substrate concentrations [9,13].

Bottom Line: In those prokaryotes, sucrose accumulation has been associated with salt acclimation, and considered as a compatible solute in low-salt tolerant strains.In the last years, functional characterizations of sucrose metabolizing enzymes, metabolic control analysis, cellular localization of gene expressions, and reverse genetic experiments have revealed that sucrose metabolism is crucial in the diazotrophic growth of heterocystic strains, and besides, that it can be connected to glycogen synthesis.This article briefly summarizes the current state of knowledge of sucrose physiological functions in modern cyanobacteria and how they might have evolved taking into account the phylogenetic analyses of sucrose enzymes.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Investigaciones en Biodiversidad y Biotecnología (INBIOTEC-CONICET) and Fundación para Investigaciones Biológicas Aplicadas (FIBA), Mar del Plata B7600DHN, Argentina. mkolman@fiba.org.ar.

ABSTRACT
In the biosphere, sucrose is mainly synthesized in oxygenic photosynthetic organisms, such as cyanobacteria, green algae and land plants, as part of the carbon dioxide assimilation pathway. Even though its central position in the functional biology of plants is well documented, much less is known about the role of sucrose in cyanobacteria. In those prokaryotes, sucrose accumulation has been associated with salt acclimation, and considered as a compatible solute in low-salt tolerant strains. In the last years, functional characterizations of sucrose metabolizing enzymes, metabolic control analysis, cellular localization of gene expressions, and reverse genetic experiments have revealed that sucrose metabolism is crucial in the diazotrophic growth of heterocystic strains, and besides, that it can be connected to glycogen synthesis. This article briefly summarizes the current state of knowledge of sucrose physiological functions in modern cyanobacteria and how they might have evolved taking into account the phylogenetic analyses of sucrose enzymes.

No MeSH data available.