The Global Influence of Sodium on Cyanobacteria in Resuscitation from Nitrogen Starvation
Dormancy and resuscitation are key to bacterial survival under fluctuating environmental conditions. In the absence of combined nitrogen sources, the non-diazotrophic model cyanobacterium <i>Synechocystis</i> sp. PCC 6803 enters into a metabolically quiescent state during a process terme...
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MDPI AG
2023-01-01
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| Series: | Biology |
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| Online Access: | https://www.mdpi.com/2079-7737/12/2/159 |
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| author | Markus Burkhardt Johanna Rapp Claudia Menzel Hannes Link Karl Forchhammer |
| author_facet | Markus Burkhardt Johanna Rapp Claudia Menzel Hannes Link Karl Forchhammer |
| author_sort | Markus Burkhardt |
| collection | DOAJ |
| description | Dormancy and resuscitation are key to bacterial survival under fluctuating environmental conditions. In the absence of combined nitrogen sources, the non-diazotrophic model cyanobacterium <i>Synechocystis</i> sp. PCC 6803 enters into a metabolically quiescent state during a process termed chlorosis. This state enables the cells to survive until nitrogen sources reappear, whereupon the cells resuscitate in a process that follows a highly orchestrated program. This coincides with a metabolic switch into a heterotrophic-like mode where glycogen catabolism provides the cells with reductant and carbon skeletons for the anabolic reactions that serve to re-establish a photosynthetically active cell. Here we show that the entire resuscitation process requires the presence of sodium, a ubiquitous cation that has a broad impact on bacterial physiology. The requirement for sodium in resuscitating cells persists even at elevated CO<sub>2</sub> levels, a condition that, by contrast, relieves the requirement for sodium ions in vegetative cells. Using a multi-pronged approach, including the first metabolome analysis of <i>Synechocystis</i> cells resuscitating from chlorosis, we reveal the involvement of sodium at multiple levels. Not only does sodium play a role in the bioenergetics of chlorotic cells, as previously shown, but it is also involved in nitrogen compound assimilation, pH regulation, and synthesis of key metabolites. |
| first_indexed | 2024-03-11T09:08:12Z |
| format | Article |
| id | doaj.art-a0d02a18db9043249cd94745ec64d74a |
| institution | Directory Open Access Journal |
| issn | 2079-7737 |
| language | English |
| last_indexed | 2024-03-11T09:08:12Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
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| spelling | doaj.art-a0d02a18db9043249cd94745ec64d74a2023-11-16T19:12:24ZengMDPI AGBiology2079-77372023-01-0112215910.3390/biology12020159The Global Influence of Sodium on Cyanobacteria in Resuscitation from Nitrogen StarvationMarkus Burkhardt0Johanna Rapp1Claudia Menzel2Hannes Link3Karl Forchhammer4Interfaculty Institute of Microbiology and Infection Medicine, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, GermanyCMFI, Bacterial Metabolomics, University of Tübingen, Auf der Morgenstelle 24, 72076 Tübingen, GermanyInterfaculty Institute of Microbiology and Infection Medicine, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, GermanyCMFI, Bacterial Metabolomics, University of Tübingen, Auf der Morgenstelle 24, 72076 Tübingen, GermanyInterfaculty Institute of Microbiology and Infection Medicine, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, GermanyDormancy and resuscitation are key to bacterial survival under fluctuating environmental conditions. In the absence of combined nitrogen sources, the non-diazotrophic model cyanobacterium <i>Synechocystis</i> sp. PCC 6803 enters into a metabolically quiescent state during a process termed chlorosis. This state enables the cells to survive until nitrogen sources reappear, whereupon the cells resuscitate in a process that follows a highly orchestrated program. This coincides with a metabolic switch into a heterotrophic-like mode where glycogen catabolism provides the cells with reductant and carbon skeletons for the anabolic reactions that serve to re-establish a photosynthetically active cell. Here we show that the entire resuscitation process requires the presence of sodium, a ubiquitous cation that has a broad impact on bacterial physiology. The requirement for sodium in resuscitating cells persists even at elevated CO<sub>2</sub> levels, a condition that, by contrast, relieves the requirement for sodium ions in vegetative cells. Using a multi-pronged approach, including the first metabolome analysis of <i>Synechocystis</i> cells resuscitating from chlorosis, we reveal the involvement of sodium at multiple levels. Not only does sodium play a role in the bioenergetics of chlorotic cells, as previously shown, but it is also involved in nitrogen compound assimilation, pH regulation, and synthesis of key metabolites.https://www.mdpi.com/2079-7737/12/2/159cyanobacteriadormancyresuscitationsodiumchlorosis |
| spellingShingle | Markus Burkhardt Johanna Rapp Claudia Menzel Hannes Link Karl Forchhammer The Global Influence of Sodium on Cyanobacteria in Resuscitation from Nitrogen Starvation Biology cyanobacteria dormancy resuscitation sodium chlorosis |
| title | The Global Influence of Sodium on Cyanobacteria in Resuscitation from Nitrogen Starvation |
| title_full | The Global Influence of Sodium on Cyanobacteria in Resuscitation from Nitrogen Starvation |
| title_fullStr | The Global Influence of Sodium on Cyanobacteria in Resuscitation from Nitrogen Starvation |
| title_full_unstemmed | The Global Influence of Sodium on Cyanobacteria in Resuscitation from Nitrogen Starvation |
| title_short | The Global Influence of Sodium on Cyanobacteria in Resuscitation from Nitrogen Starvation |
| title_sort | global influence of sodium on cyanobacteria in resuscitation from nitrogen starvation |
| topic | cyanobacteria dormancy resuscitation sodium chlorosis |
| url | https://www.mdpi.com/2079-7737/12/2/159 |
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