The essential role of sodium bioenergetics and ATP homeostasis in the developmental transitions of a cyanobacterium

Doello, Sofia; Burkhardt, Markus; Forchhammer, Karl

doi:10.1016/j.cub.2021.01.065

Cited by 16 publications

(19 citation statements)

References 36 publications

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“…Bis-(1,3-Dibutylbarbituric Acid)-trimethine oxonol (DiBAC4(3)) was used as described in ( Doello et al, 2021 ). 190 μL of cultures at timepoints 24 and 48 h after IPTG induction was stained for 30 min in the dark at RT with 10 μM DiBAC4(3) dissolved in dimethyl sulfoxide (DMSO).…”

Section: Methodsmentioning

confidence: 99%

Pleiotropic effects of PipX, PipY, or RelQ overexpression on growth, cell size, photosynthesis, and polyphosphate accumulation in the cyanobacterium Synechococcus elongatus PCC7942

Llop

Labella²,

Borisova³

et al. 2023

Front. Microbiol.

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The cyanobacterial protein PipY belongs to the Pyridoxal-phosphate (PLP)-binding proteins (PLPBP/COG0325) family of pyridoxal-phosphate-binding proteins, which are represented in all three domains of life. These proteins share a high degree of sequence conservation, appear to have purely regulatory functions, and are involved in the homeostasis of vitamin B6 vitamers and amino/keto acids. Intriguingly, the genomic context of the pipY gene in cyanobacteria connects PipY with PipX, a protein involved in signaling the intracellular energy status and carbon-to-nitrogen balance. PipX regulates its cellular targets via protein–protein interactions. These targets include the PII signaling protein, the ribosome assembly GTPase EngA, and the transcriptional regulators NtcA and PlmA. PipX is thus involved in the transmission of multiple signals that are relevant for metabolic homeostasis and stress responses in cyanobacteria, but the exact function of PipY is still elusive. Preliminary data indicated that PipY might also be involved in signaling pathways related to the stringent stress response, a pathway that can be induced in the unicellular cyanobacterium Synechococcus elongatus PCC7942 by overexpression of the (p)ppGpp synthase, RelQ. To get insights into the cellular functions of PipY, we performed a comparative study of PipX, PipY, or RelQ overexpression in S. elongatus PCC7942. Overexpression of PipY or RelQ caused similar phenotypic responses, such as growth arrest, loss of photosynthetic activity and viability, increased cell size, and accumulation of large polyphosphate granules. In contrast, PipX overexpression decreased cell length, indicating that PipX and PipY play antagonistic roles on cell elongation or cell division. Since ppGpp levels were not induced by overexpression of PipY or PipX, it is apparent that the production of polyphosphate in cyanobacteria does not require induction of the stringent response.

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Section: Methodsmentioning

confidence: 99%

Pleiotropic effects of PipX, PipY, or RelQ overexpression on growth, cell size, photosynthesis, and polyphosphate accumulation in the cyanobacterium Synechococcus elongatus PCC7942

Llop

Labella²,

Borisova³

et al. 2023

Front. Microbiol.

Self Cite

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“…To better understand the role of Na + energetics in energy metabolism, we investigated cell growth after adding either a Na + -specific ionophore monensin 19,20 , a protonophore DTHB 21 , or a typical F-type ATP synthase inhibitor DCCD 22 to the respective culture medium. If Na + fluxes were coupled to ATP synthesis, the collapse of the Na + transmembrane gradient caused by monensin should lead to growth arrest due to the inhibition of ATP synthesis.…”

Section: Resultsmentioning

confidence: 99%

“…Only recently, although not directly related to N 2 fixation, a study using Synechocystis sp. PCC 6803 reported that N-starved cells engage in Na + energetics for ATP synthesis for maintaining viability and to awaken from dormancy 20 . These reports suggest that Na + energetics may be more widespread in cyanobacteria than commonly thought.…”

Section: Discussionmentioning

confidence: 99%

Unicellular cyanobacteria rely on sodium energetics to fix N₂

Tang,

Cheng,

Liu

et al. 2024

Preprint

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Diazotrophic cyanobacteria can thrive in combined nitrogen (N)-limited environments due to their ability to fix nitrogen gas (N2) from the atmosphere. Despite this, they occur in low abundance in N-limited coastal waters, which represents an ecological paradox1–3. One hypothesis is that this is partly due to elevated salinity (> 10 g/L NaCl), which inhibits cyanobacterial N2fixation2,3. Here we show that N2fixation in a unicellular coastal cyanobacterium is not inhibited but rather exclusively dependent on sodium (Na+) ions. In N-deficient environments, both N2fixation and population growth were significantly inhibited at low NaCl concentrations (< 4 g/L). Additional experiments indicated that sodium energetics, rather than proton energetics, is necessary for N2fixation, as Na+deficiency resulted in insufficient ATP supply for N2fixation. We show that this is due to the non-functioning Na+-coupled ATP synthase, which we found to be likely coupled to anaerobic rather than aerobic respiration. Sequence alignment analysis of the ion-coupling site of the ATP synthase revealed a high prevalence of Na+energetics in cyanobacteria, with all unicellular N2fixers capable of Na+energetics. This suggests a critical role for sodium energetics in cyanobacteria. It also raises the possibility that sodium energetics is not as rare as thought, but that we may have underestimated the prevalence and importance of sodium energetics in other organisms. Finally, the low abundance of diazotrophic unicellular cyanobacteria in coastal waters may be due to insufficient NaCl levels to support N2-fixation during periods of growth-supporting high temperatures. This provides another perspective on the regulation of the oceanic N cycle that needs to be considered in times of global climate change. Changes in current patterns could lead to an overlap of periods optimal for N2fixation and population growth, likely resulting in dense cyanobacterial blooms.

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“…Whether there is a metabolic connection between the hydrogenase and the Na + -ATPase remains to be investigated. In addition to a possible halotolerance function, nitrogen-starved cells of Synechocystis PCC 6803 use ATPase to produce a sodium motive force that maintains sufficient levels of ATP for survival during metabolic dormancy [ 56 ]. Both sodium bioenergetics and glycogen catabolism are important during the resumption of growth in Synechocystis PCC 6803 following nitrogen starvation [ 56 ], and future work could address if hydrogenase activity also contributes.…”

Section: Resultsmentioning

confidence: 99%

Genomic and Functional Variation of the Chlorophyll d-Producing Cyanobacterium Acaryochloris marina

et al. 2022

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The Chlorophyll d-producing cyanobacterium Acaryochloris marina is widely distributed in marine environments enriched in far-red light, but our understanding of its genomic and functional diversity is limited. Here, we take an integrative approach to investigate A. marina diversity for 37 strains, which includes twelve newly isolated strains from previously unsampled locations in Europe and the Pacific Northwest of North America. A genome-wide phylogeny revealed both that closely related A. marina have migrated within geographic regions and that distantly related A. marina lineages can co-occur. The distribution of traits mapped onto the phylogeny provided evidence of a dynamic evolutionary history of gene gain and loss during A. marina diversification. Ancestral genes that were differentially retained or lost by strains include plasmid-encoded sodium-transporting ATPase and bidirectional NiFe-hydrogenase genes that may be involved in salt tolerance and redox balance under fermentative conditions, respectively. The acquisition of genes by horizontal transfer has also played an important role in the evolution of new functions, such as nitrogen fixation. Together, our results resolve examples in which genome content and ecotypic variation for nutrient metabolism and environmental tolerance have diversified during the evolutionary history of this unusual photosynthetic bacterium.

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The essential role of sodium bioenergetics and ATP homeostasis in the developmental transitions of a cyanobacterium

Abstract: Highlights d Synechocystis engages sodium bioenergetics during nitrogen starvation d Sodium-dependent ATP synthesis is only essential during metabolic dormancy d ATP levels are finely tuned according to the metabolic requirements

Cited by 16 publications

References 36 publications

Pleiotropic effects of PipX, PipY, or RelQ overexpression on growth, cell size, photosynthesis, and polyphosphate accumulation in the cyanobacterium Synechococcus elongatus PCC7942

Pleiotropic effects of PipX, PipY, or RelQ overexpression on growth, cell size, photosynthesis, and polyphosphate accumulation in the cyanobacterium Synechococcus elongatus PCC7942

Unicellular cyanobacteria rely on sodium energetics to fix N₂

Genomic and Functional Variation of the Chlorophyll d-Producing Cyanobacterium Acaryochloris marina

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The essential role of sodium bioenergetics and ATP homeostasis in the developmental transitions of a cyanobacterium

Abstract: Highlights d Synechocystis engages sodium bioenergetics during nitrogen starvation d Sodium-dependent ATP synthesis is only essential during metabolic dormancy d ATP levels are finely tuned according to the metabolic requirements

Cited by 16 publications

References 36 publications

Pleiotropic effects of PipX, PipY, or RelQ overexpression on growth, cell size, photosynthesis, and polyphosphate accumulation in the cyanobacterium Synechococcus elongatus PCC7942

Pleiotropic effects of PipX, PipY, or RelQ overexpression on growth, cell size, photosynthesis, and polyphosphate accumulation in the cyanobacterium Synechococcus elongatus PCC7942

Unicellular cyanobacteria rely on sodium energetics to fix N2

Genomic and Functional Variation of the Chlorophyll d-Producing Cyanobacterium Acaryochloris marina

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Unicellular cyanobacteria rely on sodium energetics to fix N₂