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Chlorophyll biosynthesis under the control of arginine metabolism

ABSTRACT: In natural environments, photosynthetic organisms adjust their metabolism to cope with the fluctuating availability of combined nitrogen-sources, a growth limiting factor. For the acclimation, the dynamic degradation/synthesis of tetrapyrrolic pigments as well as of the amino acid arginine is pivotal; however, there was no evidence that these processes could be functionally coupled. Using co-immunopurification and spectral shift assays we found that in the cyanobacterium Synechocystis sp. PCC 6803 the arginine-related ArgD and CphB enzymes form protein complexes with Gun4, an essential factor for chlorophyll biosynthesis. Gun4 binds ArgD with high affinity, and the ArgD-Gun4 complex strongly accumulates in cells supplemented with ornithine, a key intermediate of the arginine pathway. Elevated ornithine levels restricted de novo synthesis of tetrapyrrolic pigments, which arrested the recovery from nitrogen deficiency. Our data reveals a direct cross-talk between tetrapyrrole biosynthesis and arginine metabolism that clarifies the importance of balancing photosynthetic pigment synthesis with nitrogen homeostasis.

INSTRUMENT(S): timsTOF Pro

ORGANISM(S): Synechocystis Sp. Pcc 6803 (ncbitaxon:1148)

SUBMITTER: Roman Sobotka

PROVIDER: MSV000091280 | MassIVE | Tue Feb 14 07:46:00 GMT 2023

SECONDARY ACCESSION(S): PXD040117

REPOSITORIES: MassIVE

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Chlorophyll biosynthesis under the control of arginine metabolism.

Project description:In natural environments, photosynthetic organisms adjust their metabolism to cope with the fluctuating availability of combined nitrogen sources, a growth-limiting factor. For acclimation, the dynamic degradation/synthesis of tetrapyrrolic pigments, as well as of the amino acid arginine, is pivotal; however, there has been no evidence that these processes could be functionally coupled. Using co-immunopurification and spectral shift assays, we found that in the cyanobacterium Synechocystis sp. PCC 6803, the arginine metabolism-related ArgD and CphB enzymes form protein complexes with Gun4, an essential protein for chlorophyll biosynthesis. Gun4 binds ArgD with high affinity, and the Gun4-ArgD complex accumulates in cells supplemented with ornithine, a key intermediate of the arginine pathway. Elevated ornithine levels restricted de novo synthesis of tetrapyrroles, which arrested the recovery from nitrogen deficiency. Our data reveal a direct crosstalk between tetrapyrrole biosynthesis and arginine metabolism that highlights the importance of balancing photosynthetic pigment synthesis with nitrogen homeostasis.

2024-03-12 | MTBLS8336 | MetaboLights

TrxA-mediated regulation of protein synthesis contributes to the maintenance of carbon and nitrogen balance in cyanobacteria.

Project description:Thioredoxins play an essential role in regulating enzyme activity upon response to environmental changes, especially in photosynthetic organisms. These are crucial for the regulation of metabolism in cyanobacteria, but the key central processes redox-regulated remain to be determined. Physiological, metabolic and transcriptomic characterization of a conditional mutant of the essential trxA gene in Synechocystis (STXA2) revealed that reduced TrxA levels alter cell morphology and enter in a dormant-like state. TrxA depletion in the STXA2 strain inhibited protein synthesis and led to changes in amino acid pools and nitrogen/carbon reserve polymers, accompanied by oxidation of the Elongation Factor EF-Tu. Transcriptomic analysis of TrxA depletion in STXA2 showed a robust transcriptional response. Genes that responded negatively were grouped in a large cluster and were directly related to photosynthesis, ATP synthesis and CO2 fixation, while genes that responded positively were grouped in different clusters and related to respiratory electron transport, carotenoids synthesis, amino acid metabolism and protein degradation, among others. Regulation of cyanobacterial metabolism is complex and fine-tuned, our results link TrxA to the switch from anabolic to maintenance metabolism in cyanobacteria, regulating carbon and nitrogen balance.

2023-09-24 | GSE243518 | GEO

The response of Chlamydomonas reinhardtii to nitrogen deprivation: a systems biology analysis

Project description:Drastic alteration in macronutrients causes large changes in gene expression in the photosynthetic unicellular alga Chlamydomonas reinhardtii. Preliminary data suggested that cells follow a biphasic response to this change hinging on the initiation of lipid accumulation, and we hypothesized that drastic repatterning of metabolism also followed this biphasic modality. To test this hypothesis, transcriptomic, proteomic, and metabolite changes that occur under nitrogen (N) deprivation were analyzed. Eight sampling times were selected covering the progressive slowing of growth and induction of oil synthesis between 4 and 6 h after N deprivation. Results of the combined, systems-level investigation indicated that C. reinhardtii cells sense and respond on a large scale within 30 min to a switch to N-deprived conditions turning on a largely gluconeogenic metabolic state, which then transitions to a glycolytic stage between 4 and 6 h after N depletion. This nitrogen-sensing system is transduced to carbon- and nitrogen-responsive pathways, leading to down-regulation of carbon assimilation and chlorophyll biosynthesis, and an increase in nitrogen metabolism and lipid biosynthesis. For example, the expression of nearly all the enzymes for assimilating nitrogen from ammonium, nitrate, nitrite, urea, formamide/acetamide, purines, pyrimidines, polyamines, amino acids and proteins increased significantly. Although arginine biosynthesis enzymes were also rapidly up-regulated, arginine pool size changes and isotopic labeling results indicated no increased flux through this pathway.

2015-06-17 | PXD002377 | Pride

RNA-seq analysis of recombinant Synechocystis sp. 6803 provides important insights for understanding polyhydroxyalkanoate production in cyanobacteria under photoautotrophic conditions

Project description:The direct photosynthetic production of polyhydroxyalkanoate in cyanobacteria was improved by increasing carbon flux to biosynthetic pathway and introducing enzyme with higher activity. To understand the global transcriptional changes under photoautotrophic PHA biosynthesis conditions, RNA-seq analysis was performed. Transcriptomes of recombinant Synechocystis sp. with different PHA-producing potential (three strains, two biological replicates for each strain) were analyzed.

2013-12-01 | E-GEOD-50688 | biostudies-arrayexpress

The sRNA NsiR4 is involved in nitrogen assimilation control in cyanobacteria by targeting glutamine synthetase inactivating factor IF7

Project description:Glutamine synthetase (GS), a key enzyme in biological nitrogen assimilation, is regulated in multiple ways in response to varying nitrogen sources and levels. Here we show a small regulatory RNA, NsiR4 (nitrogen stress induced RNA 4), which plays an important role in the regulation of GS in cyanobacteria. NsiR4 expression in the unicellular Synechocystis sp. PCC 6803 and in the filamentous, nitrogen-fixing Anabaena sp. PCC 7120 is stimulated through nitrogen-limitation via NtcA, the global transcriptional regulator of genes involved in nitrogen metabolism. NsiR4 is widely conserved throughout the cyanobacterial phylum, suggesting a conserved function. In silico target prediction, transcriptome profiling upon pulse overexpression and site-directed mutagenesis experiments using a heterologous reporter system showed that NsiR4 interacts with the 5’UTR of gifA mRNA, which encodes glutamine synthetase inactivating factor IF7. In Synechocystis, we observed an inverse relationship between the levels of NsiR4 and the accumulation of IF7 in vivo. This NsiR4-dependent modulation of gifA (IF7) mRNA accumulation influenced the glutamine pool and thus NH4+ assimilation via glutamine synthetase. As a second target, we identified ssr1528, a hitherto uncharacterized nitrogen-regulated gene. Competition experiments between wild type and an NsiR4 knock-out mutant showed that the lack of NsiR4 led to decreased acclimation capabilities of Synechocystis towards oscillating nitrogen levels. These results suggest a role for NsiR4 in the regulation of nitrogen metabolism in cyanobacteria, especially for the adaptation to rapid changes in available nitrogen sources and concentrations. NsiR4 is the first identified bacterial sRNA regulating the primary assimilation of a macronutrient.

2015-10-20 | GSE73840 | GEO

Elucidating the direct target regulon of NtcA during the early acclimation to nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803 [RNA-Seq]

Project description:Cyanobacteria are oxygenic photoautotrophs responsible for a substantial proportion of nitrogen fixation and primary production in the hydrosphere. Non-nitrogen fixing cyanobacteria, such as Synechocystis sp. PCC 6803, depend of the availability of nitrogenized species to survive. Therefore, an intricate regulatory network around the transcriptional factor NtcA maintains the homeostasis of nitrogen in these organisms. The mechanisms controlling NtcA activity are well understood but a comprehensive study of its regulon is missing in Synechocystis. To define NtcA regulon during the early stage of nitrogen starvation, we have performed chromatin immunoprecipitation followed by sequencing (ChiP-seq), in parallel with genome level transcriptome analysis (RNA-seq). By combining both methods we assigned 51 activated and 28 repressed genes directly by NtcA. Most of direct targets included genes involved in nitrogen and carbon metabolism and photosynthesis. NtcA regulon also included 8 ncRNAs, of which ncr0710, Syr6 and NsiR7 were experimentally validated. Intriguingly, we identified several NtcA intragenic binding sites suggesting that NtcA can modulate transcriptional expression by binding along the whole transcript and not only in the promoter region as previously though. Finally, the transcriptional implication of PipX was analyzed in some NtcA-targets genes, revealing that PipX assists NtcA in the global nitrogen regulation in Synechocystis.

2017-10-01 | GSE97289 | GEO

Elucidating the direct target regulon of NtcA during the early acclimation to nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803 [ChIP-Seq]

2017-10-01 | GSE97282 | GEO

RS07910/07915 TCS multipath regulates clavulanic acid metabolic pathways in Streptomyces clavuligerus F613-1

Project description:Streptomyces clavuligerus F613-1 produces a clinically important β-lactamase inhibitor, clavulanic acid (CA). The biosynthesis pathway of CA has been basically elucidated, however, the global regulation of CA biosynthesis remains unclear. In order to further elucidate the regulatory mechanism of clavulanic acid synthesis, TCS RS07910/07915 which is next to the CA biosynthetic gene cluster was deleted in Streptomyces clavuligerus. F613-1. Deletion of RS07910/07915 results in decreased the production of CA, but the phenotype was not affected. Both the transcriptome and ChIP-seq data revealed that the TCS RS07910/07915 mainly regulate genes involved in primary metabolism (such as fatty acid degradation, glyceraldehyde 3-phosphate (G3P) metabolism, arginine biosynthesis) and CA biosynthesis. EMSA assays revealed that RS07915 could bind to the promoter fragments of argG, argC, oat1, oat2, ceaS1 and claR in vitro, indicating that RS07915 could direct regulate the biosynthesis genes of arginine and CA. This study indicated that RS07910/07915 is a pleiotropy regulatory TCS, RS07910/07915 could directly affect the biosynthesis of CA, and indirectly affect CA production through affecting primary metabolism of arginine and G3P (precursors of CA).

2018-08-30 | GSE119208 | GEO

Expression of formate-THF ligase has a deep impact on primary metabolism of Synechocystis sp. PCC 6803

Project description:The introduction of alternative CO2-fixing pathways such as formate synthesis and assimilation may improve the efficiency of biological carbon fixation that appears to be limited by the enzymatic properties of ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO). Here we aimed to establish a formate assimilation pathway in the model cyanobacterium Synechocystis sp. PCC 6803. The formate-tetrahydrofolate ligase (FTL) from Methylobacterium extorquens AM1 was expressed in Synechocystis to enable formate assimilation and reduce the loss of fixed carbon in the photorespiratory pathway. Transgenic strains accumulated serine and 3-phosphoglycerate, and consumed more 2-phosphoglycolate and glycine, which seemed to reflect the efficient utilization of formate. However, labelling experiments showed that the serine accumulation was not due to the expected incorporation of formate. DNA-microarray experiments were performed to analyze possible transcriptome changes due to ftl expression. Marked changes in expression of genes encoding proteins associated with serine biosynthesis and enzymes involved in nitrogen and C1 metabolism revealed that ftl expression had a regulatory impact on these metabolic routes. Our results indicate that the expression of new pathways could have a severe impact on the cellular regulatory network, which hampers the establishment of newly designed pathways.

2020-01-17 | GSE143785 | GEO

6S RNA plays a role in recovery from nitrogen depletion in Synechocystis sp. PCC 6803

Project description:Background: The 6S RNA is a global transcriptional riboregulator, which is exceptionally widespread among most bacterial phyla. While its role is well-characterized in some heterotrophic bacteria, we subjected a cyanobacterial homolog to functional analysis, thereby extending the scope of 6S RNA action to the special challenges of photoautotrophic lifestyles. Results: Physiological characterization of a 6S RNA deletion strain (ΔssaA) demonstrates a delay in the recovery from nitrogen starvation. Significantly decelerated phycobilisome reassembly and glycogen degradation are accompanied with reduced photosynthetic activity compared to the wild type. Transcriptome profiling further revealed that predominantly genes encoding photosystem components, ATP synthase, phycobilisomes and ribosomal proteins were negatively affected in ΔssaA. In vivo pull-down studies of the RNA polymerase complex indicated that the presence of 6S RNA promotes the recruitment of the cyanobacterial housekeeping σ factor SigA, concurrently supporting dissociation of group 2 σ factors during recovery from nitrogen starvation. Conclusions: The combination of genetic, physiological and biochemical studies reveals the homologue of 6S RNA as an integral part of the cellular response of Synechocystis sp. PCC 6803 to changing nitrogen availability. According to these results, 6S RNA supports a rapid acclimation to changing nitrogen supply by accelerating the switch from group 2 σ factors SigB, SigC and SigE to SigA-dependent transcription. We therefore introduce the cyanobacterial 6S RNA as a novel candidate regulator of RNA polymerase sigma factor recruitment in Synechocystis sp. PCC 6803. Further studies on mechanistic features of the postulated interaction should shed additional light on the complexity of transcriptional regulation in cyanobacteria.

2016-06-16 | GSE83387 | GEO

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