Sucrose in Cyanobacteria: From a Salt-Response Molecule to Play a Key Role in Nitrogen Fixation

Kolman, María A.; Nishi, Carolina N.; Perez-Cenci, Macarena; Salerno, Graciela L.

doi:10.3390/life5010102

Cited by 47 publications

(60 citation statements)

References 71 publications

(130 reference statements)

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“…Respiration in the heterocysts requires a source of reductant that is received from the adjacent vegetative cells. In Anabaena , sucrose appears to be the main source of intercellularly transferred reductant, since inactivation of an invertase, InvB, expressed specifically in the heterocysts blocks diazotrophic growth (López‐Igual et al ., ; Vargas et al ., ; reviewed in Kolman et al ., ). Invertases irreversibly cleave sucrose into glucose and fructose, and the oxidative pentose phosphate pathway mediates sugar catabolism in the heterocysts (Summers et al ., ).…”

Section: N2 Fixation and The Heterocystmentioning

confidence: 97%

Genetic responses to carbon and nitrogen availability in Anabaena

Herrero

Flores

2018

Environmental Microbiology

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Heterocyst-forming cyanobacteria are filamentous organisms that perform oxygenic photosynthesis and CO fixation in vegetative cells and nitrogen fixation in heterocysts, which are formed under deprivation of combined nitrogen. These organisms can acclimate to use different sources of nitrogen and respond to different levels of CO . Following work mainly done with the best studied heterocyst-forming cyanobacterium, Anabaena, here we summarize the mechanisms of assimilation of ammonium, nitrate, urea and N , the latter involving heterocyst differentiation, and describe aspects of CO assimilation that involves a carbon concentration mechanism. These processes are subjected to regulation establishing a hierarchy in the assimilation of nitrogen sources -with preference for the most reduced nitrogen forms- and a dependence on sufficient carbon. This regulation largely takes place at the level of gene expression and is exerted by a variety of transcription factors, including global and pathway-specific transcriptional regulators. NtcA is a CRP-family protein that adjusts global gene expression in response to the C-to-N balance in the cells, and PacR is a LysR-family transcriptional regulator (LTTR) that extensively acclimates the cells to oxygenic phototrophy. A cyanobacterial-specific transcription factor, HetR, is involved in heterocyst differentiation, and other LTTR factors are specifically involved in nitrate and CO assimilation.

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Section: N2 Fixation and The Heterocystmentioning

confidence: 97%

Genetic responses to carbon and nitrogen availability in Anabaena

Herrero

Flores

2018

Environmental Microbiology

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“…The evolutionary origin of enzymes from sucrose metabolism in proteobacteria has been previously discussed (4,5,8,64). The evolution of sucrose synthases in cyanobacteria, proteobacteria, and plants is not yet fully understood, but most likely it involved horizontal gene transfers.…”

Section: Ii) Sugar-binding Gt-b(a) Domainmentioning

confidence: 99%

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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“…In the present study, 70 proteins associated with carbohydrate metabolism have been identified in the three strains. Sucrose plays a critical role in carbon flux modulation in the nitrogen‐fixing filaments of Anabaena . Sucrose biosynthesis can be performed both in vegetative cells and heterocysts .…”

Section: Resultsmentioning

confidence: 99%

Proteome Analysis of Enriched Heterocysts from Two Hydrogenase Mutants from Anabaena sp. PCC 7120

et al. 2019

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Cyanobacteria are oxygenic photosynthetic prokaryotes and play a crucial role in the Earth's carbon and nitrogen cycles. The photoautotrophic cyanobacterium Anabaena sp. PCC 7120 has the ability to fix atmospheric nitrogen in heterocysts and produce hydrogen as a byproduct through a nitrogenase. In order to improve hydrogen production, mutants from Anabaena sp. PCC 7120 are constructed by inactivation of the uptake hydrogenase (ΔhupL) and the bidirectional hydrogenase (ΔhoxH) in previous studies. Here the proteomic differences of enriched heterocysts between these mutants cultured in N2‐fixing conditions are investigated. Using a label‐free quantitative proteomics approach, a total of 2728 proteins are identified and it is found that 79 proteins are differentially expressed in the ΔhupL and 117 proteins in the ΔhoxH variant. The results provide for the first time comprehensive information on proteome regulation of the uptake hydrogenase and the bidirectional hydrogenase, as well as systematic data on the hydrogen related metabolism in Anabaena sp. PCC 7120.

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Sucrose in Cyanobacteria: From a Salt-Response Molecule to Play a Key Role in Nitrogen Fixation

Cited by 47 publications

References 71 publications

Genetic responses to carbon and nitrogen availability in Anabaena

Genetic responses to carbon and nitrogen availability in Anabaena

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

Proteome Analysis of Enriched Heterocysts from Two Hydrogenase Mutants from Anabaena sp. PCC 7120

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