Differential roles of alkaline/neutral invertases in Nostoc sp. PCC 7120: Inv-B isoform is essential for diazotrophic growth

Vargas, Walter M.; Nishi, Carolina N.; Giarrocco, Laura Estela; Salerno, Graciela L.

doi:10.1007/s00425-010-1288-5

Cited by 42 publications

(39 citation statements)

References 35 publications

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“…Sucrose is thought to be the principal form of reduced carbon transferred to heterocysts during diazotrophic growth [4, 8, 9, 90–92]. In cyanobacteria sucrose is synthesized by sucrose-phosphate (sucrose-P) synthase and sucrose-P phosphatase [93, 94].…”

Section: Resultsmentioning

confidence: 99%

“…N 2 fixed in heterocysts is assimilated through the glutamine synthetase-glutamate synthase (GS-GOGAT) pathway, and glutamine is considered a main nitrogenous product transported to vegetative cells. In exchange, vegetative cells have been thought to transfer sucrose and glutamate to the heterocysts [6–9]. In the light, ferredoxin reduced by photosystem I (PS I) is the likely source of electrons for N 2 fixation [10], but the metabolic pathway or pathways that transfer electrons to PS I in heterocysts are not known.…”

Section: Introductionmentioning

confidence: 99%

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Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically

et al. 2013

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BackgroundWhen the filamentous cyanobacterium Anabaena variabilis grows aerobically without combined nitrogen, some vegetative cells differentiate into N2-fixing heterocysts, while the other vegetative cells perform photosynthesis. Microarrays of sequences within protein-encoding genes were probed with RNA purified from extracts of vegetative cells, from isolated heterocysts, and from whole filaments to investigate transcript levels, and carbon and energy metabolism, in vegetative cells and heterocysts in phototrophic, mixotrophic, and heterotrophic cultures.ResultsHeterocysts represent only 5% to 10% of cells in the filaments. Accordingly, levels of specific transcripts in vegetative cells were with few exceptions very close to those in whole filaments and, also with few exceptions (e.g., nif1 transcripts), levels of specific transcripts in heterocysts had little effect on the overall level of those transcripts in filaments. In phototrophic, mixotrophic, and heterotrophic growth conditions, respectively, 845, 649, and 846 genes showed more than 2-fold difference (p < 0.01) in transcript levels between vegetative cells and heterocysts. Principal component analysis showed that the culture conditions tested affected transcript patterns strongly in vegetative cells but much less in heterocysts. Transcript levels of the genes involved in phycobilisome assembly, photosynthesis, and CO2 assimilation were high in vegetative cells in phototrophic conditions, and decreased when fructose was provided. Our results suggest that Gln, Glu, Ser, Gly, Cys, Thr, and Pro can be actively produced in heterocysts. Whether other protein amino acids are synthesized in heterocysts is unclear. Two possible components of a sucrose transporter were identified that were upregulated in heterocysts in two growth conditions. We consider it likely that genes with unknown function represent a larger fraction of total transcripts in heterocysts than in vegetative cells across growth conditions.ConclusionsThis study provides the first comparison of transcript levels in heterocysts and vegetative cells from heterocyst-bearing filaments of Anabaena. Although the data presented do not give a complete picture of metabolism in either type of cell, they provide a metabolic scaffold on which to build future analyses of cell-specific processes and of the interactions of the two types of cells.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-14-759) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically

et al. 2013

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“…Invertase catalyzes the irreversible hydrolysis of sucrose into hexoses. The invB gene is highly expressed in heterocysts and is essential for diazotrophic growth (13,14).…”

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Sucrose Synthesis in the Nitrogen-Fixing Cyanobacterium Anabaena sp. Strain PCC 7120 Is Controlled by the Two-Component Response Regulator OrrA

Ehira

Kimura

Miyazaki

et al. 2014

Appl Environ Microbiol

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dThe filamentous, nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120 accumulates sucrose as a compatible solute against salt stress. Sucrose-phosphate synthase activity, which is responsible for the sucrose synthesis, is increased by salt stress, but the mechanism underlying the regulation of sucrose synthesis remains unknown. In the present study, a response regulator, OrrA, was shown to control sucrose synthesis. Expression of spsA, which encodes a sucrose-phosphate synthase, and susA and susB, which encode sucrose synthases, was induced by salt stress. In the orrA disruptant, salt induction of these genes was completely abolished. The cellular sucrose level of the orrA disruptant was reduced to 40% of that in the wild type under salt stress conditions. Moreover, overexpression of orrA resulted in enhanced expression of spsA, susA, and susB, followed by accumulation of sucrose, without the addition of NaCl. We also found that SigB2, a group 2 sigma factor of RNA polymerase, regulated the early response to salt stress under the control of OrrA. It is concluded that OrrA controls sucrose synthesis in collaboration with SigB2.

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“…An exchange of glutamine (transferred from heterocysts to vegetative cells) for glutamate (transferred from vegetative cells to heterocysts) is thought to take place (4,5). Additionally, sucrose (6)(7)(8)(9) and alanine (10,11) appear to be transferred from vegetative cells to heterocysts, and ␤-aspartyl-arginine appears to be transferred from heterocysts to vegetative cells (12).…”

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Functional Dependence between Septal Protein SepJ from Anabaena sp. Strain PCC 7120 and an Amino Acid ABC-Type Uptake Transporter

2015

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In the diazotrophic filaments of heterocyst-forming cyanobacteria, two different cell types, the CO 2 -fixing vegetative cells and the N 2 -fixing heterocysts, exchange nutrients, including some amino acids. In the model organism Anabaena sp. strain PCC 7120, the SepJ protein, composed of periplasmic and integral membrane (permease) sections, is located at the intercellular septa joining adjacent cells in the filament. The unicellular cyanobacterium Synechococcus elongatus strain PCC 7942 bears a gene, Synpcc7942_1024 (here designated dmeA), encoding a permease homologous to the SepJ permease domain. Synechococcus strains lacking dmeA or lacking dmeA and expressing Anabaena sepJ were constructed. The Synechococcus dmeA mutant showed a significant 22 to 32% decrease in the uptake of aspartate, glutamate, and glutamine, a phenotype that could be partially complemented by Anabaena sepJ. Synechococcus mutants of an ATP-binding-cassette (ABC)-type transporter for polar amino acids showed >98% decreased uptake of glutamate irrespective of the presence of dmeA or Anabaena sepJ in the same strain. Thus, Synechococcus DmeA or Anabaena SepJ is needed to observe full (or close to full) activity of the ABC transporter. An Anabaena sepJ deletion mutant was significantly impaired in glutamate and aspartate uptake, which also in this cyanobacterium requires the activity of an ABC-type transporter for polar amino acids. SepJ appears therefore to generally stimulate the activity of cyanobacterial ABC-type transporters for polar amino acids. Conversely, an Anabaena mutant of three ABC-type transporters for amino acids was impaired in the intercellular transfer of 5-carboxyfluorescein, a SepJ-related property. Our results unravel possible functional interactions in transport elements important for diazotrophic growth. IMPORTANCEMembrane transporters are essential for many aspects of cellular life, from uptake and export of substances in unicellular organisms to intercellular molecular exchange in multicellular organisms. Heterocyst-forming cyanobacteria such as Anabaena represent a unique case of multicellularity, in which two cell types exchange nutrients and regulators. The SepJ protein located at the intercellular septa in the filaments of Anabaena contains a permease domain of the drug/metabolite transporter (DMT) superfamily that somehow contributes to intercellular molecular transfer. In this work, we have found that SepJ stimulates the activity of a polar amino acid uptake transporter of the ATP-binding-cassette (ABC) superfamily, which could itself affect an intercellular transfer activity related to SepJ, thus unraveling possible functional interactions between these different transporters. Some cyanobacteria grow as chains of cells known as filaments or trichomes that, when incubated in the absence of a source of combined nitrogen, present two cell types: vegetative cells that perform oxygenic photosynthesis and fix carbon dioxide and heterocysts that perform N 2 fixation (1-3). In species of the genera Anabaena ...

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Differential roles of alkaline/neutral invertases in Nostoc sp. PCC 7120: Inv-B isoform is essential for diazotrophic growth

Cited by 42 publications

References 35 publications

Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically

Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically

Sucrose Synthesis in the Nitrogen-Fixing Cyanobacterium Anabaena sp. Strain PCC 7120 Is Controlled by the Two-Component Response Regulator OrrA

Functional Dependence between Septal Protein SepJ from Anabaena sp. Strain PCC 7120 and an Amino Acid ABC-Type Uptake Transporter

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