The sRNA NsiR4 fine-tunes arginine synthesis in the cyanobacterium Synechocystis sp. PCC 6803 by post-transcriptional regulation of PirA
As the only oxygenic phototrophs among prokaryotes, cyanobacteria employ intricate mechanisms to regulate common metabolic pathways. These mechanisms include small protein inhibitors exerting their function by protein–protein interaction with key metabolic enzymes and regulatory small RNAs (sRNAs)....
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2022-12-01
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| Series: | RNA Biology |
| Subjects: | |
| Online Access: | http://dx.doi.org/10.1080/15476286.2022.2082147 |
| _version_ | 1797404007699841024 |
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| author | Paul Bolay Luisa Hemm Francisco J. Florencio Wolfgang R. Hess M. Isabel Muro-Pastor Stephan Klähn |
| author_facet | Paul Bolay Luisa Hemm Francisco J. Florencio Wolfgang R. Hess M. Isabel Muro-Pastor Stephan Klähn |
| author_sort | Paul Bolay |
| collection | DOAJ |
| description | As the only oxygenic phototrophs among prokaryotes, cyanobacteria employ intricate mechanisms to regulate common metabolic pathways. These mechanisms include small protein inhibitors exerting their function by protein–protein interaction with key metabolic enzymes and regulatory small RNAs (sRNAs). Here we show that the sRNA NsiR4, which is highly expressed under nitrogen limiting conditions, interacts with the mRNA of the recently described small protein PirA in the model strain Synechocystis sp. PCC 6803. In particular, NsiR4 targets the pirA 5ʹUTR close to the ribosome binding site. Heterologous reporter assays confirmed that this interaction interferes with pirA translation. PirA negatively impacts arginine synthesis under ammonium excess by competing with the central carbon/nitrogen regulator PII that binds to and thereby activates the key enzyme of arginine synthesis, N-acetyl-L-glutamate-kinase (NAGK). Consistently, ectopic nsiR4 expression in Synechocystis resulted in lowered PirA accumulation in response to ammonium upshifts, which also affected intracellular arginine pools. As NsiR4 and PirA are inversely regulated by the global nitrogen transcriptional regulator NtcA, this regulatory axis enables fine tuning of arginine synthesis and conveys additional metabolic flexibility under highly fluctuating nitrogen regimes. Pairs of small protein inhibitors and of sRNAs that control the abundance of these enzyme effectors at the post-transcriptional level appear as fundamental building blocks in the regulation of primary metabolism in cyanobacteria. |
| first_indexed | 2024-03-09T02:46:52Z |
| format | Article |
| id | doaj.art-f39f729be1dd438dbbbc4e306b590080 |
| institution | Directory Open Access Journal |
| issn | 1547-6286 1555-8584 |
| language | English |
| last_indexed | 2024-03-09T02:46:52Z |
| publishDate | 2022-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | RNA Biology |
| spelling | doaj.art-f39f729be1dd438dbbbc4e306b5900802023-12-05T16:09:51ZengTaylor & Francis GroupRNA Biology1547-62861555-85842022-12-0119181181810.1080/15476286.2022.20821472082147The sRNA NsiR4 fine-tunes arginine synthesis in the cyanobacterium Synechocystis sp. PCC 6803 by post-transcriptional regulation of PirAPaul Bolay0Luisa Hemm1Francisco J. Florencio2Wolfgang R. Hess3M. Isabel Muro-Pastor4Stephan Klähn5Helmholtz Centre for Environmental ResearchUniversity of FreiburgInstituto de Bioquímica Vegetal Y FotosíntesisUniversity of FreiburgInstituto de Bioquímica Vegetal Y FotosíntesisHelmholtz Centre for Environmental ResearchAs the only oxygenic phototrophs among prokaryotes, cyanobacteria employ intricate mechanisms to regulate common metabolic pathways. These mechanisms include small protein inhibitors exerting their function by protein–protein interaction with key metabolic enzymes and regulatory small RNAs (sRNAs). Here we show that the sRNA NsiR4, which is highly expressed under nitrogen limiting conditions, interacts with the mRNA of the recently described small protein PirA in the model strain Synechocystis sp. PCC 6803. In particular, NsiR4 targets the pirA 5ʹUTR close to the ribosome binding site. Heterologous reporter assays confirmed that this interaction interferes with pirA translation. PirA negatively impacts arginine synthesis under ammonium excess by competing with the central carbon/nitrogen regulator PII that binds to and thereby activates the key enzyme of arginine synthesis, N-acetyl-L-glutamate-kinase (NAGK). Consistently, ectopic nsiR4 expression in Synechocystis resulted in lowered PirA accumulation in response to ammonium upshifts, which also affected intracellular arginine pools. As NsiR4 and PirA are inversely regulated by the global nitrogen transcriptional regulator NtcA, this regulatory axis enables fine tuning of arginine synthesis and conveys additional metabolic flexibility under highly fluctuating nitrogen regimes. Pairs of small protein inhibitors and of sRNAs that control the abundance of these enzyme effectors at the post-transcriptional level appear as fundamental building blocks in the regulation of primary metabolism in cyanobacteria.http://dx.doi.org/10.1080/15476286.2022.2082147cyanobacterianitrogen assimilationarginine metabolismrna regulatorsrnaposttranscriptional regulation |
| spellingShingle | Paul Bolay Luisa Hemm Francisco J. Florencio Wolfgang R. Hess M. Isabel Muro-Pastor Stephan Klähn The sRNA NsiR4 fine-tunes arginine synthesis in the cyanobacterium Synechocystis sp. PCC 6803 by post-transcriptional regulation of PirA RNA Biology cyanobacteria nitrogen assimilation arginine metabolism rna regulator srna posttranscriptional regulation |
| title | The sRNA NsiR4 fine-tunes arginine synthesis in the cyanobacterium Synechocystis sp. PCC 6803 by post-transcriptional regulation of PirA |
| title_full | The sRNA NsiR4 fine-tunes arginine synthesis in the cyanobacterium Synechocystis sp. PCC 6803 by post-transcriptional regulation of PirA |
| title_fullStr | The sRNA NsiR4 fine-tunes arginine synthesis in the cyanobacterium Synechocystis sp. PCC 6803 by post-transcriptional regulation of PirA |
| title_full_unstemmed | The sRNA NsiR4 fine-tunes arginine synthesis in the cyanobacterium Synechocystis sp. PCC 6803 by post-transcriptional regulation of PirA |
| title_short | The sRNA NsiR4 fine-tunes arginine synthesis in the cyanobacterium Synechocystis sp. PCC 6803 by post-transcriptional regulation of PirA |
| title_sort | srna nsir4 fine tunes arginine synthesis in the cyanobacterium synechocystis sp pcc 6803 by post transcriptional regulation of pira |
| topic | cyanobacteria nitrogen assimilation arginine metabolism rna regulator srna posttranscriptional regulation |
| url | http://dx.doi.org/10.1080/15476286.2022.2082147 |
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