Quantitative Proteomics Reveals the Protein Regulatory Network of <i>Anabaena</i> sp. PCC 7120 under Nitrogen Deficiency

Zhang, Qi; Yu, Shengchao; Wang, Qiang; Yang, Mingkun; Ge, Feng

doi:10.1021/acs.jproteome.1c00302

“…Here, we found that upstream of pecB , there are two putative RpaA binding sites ( P value = 1.5 × 10 −5 , Table S1). Since neither the abundance of RpaA nor its transcription decreases as a result of nitrogen deprivation ( 18 , 38 ), lower levels of pecBACEF transcription may be effected by a reduction in the levels of the active phosphorylated form (RpaA~P), which may be mediated by SasA and CikA in Anabaena as in S. elongatus ( 39 ). SasA is regulated in S. elongatus by the phycobilisome-associated B protein (RpaB), which is involved in the integration of temporal and environmental information and stress ( 40 ).…”

Section: Discussionmentioning

confidence: 99%

Spatio-temporal coherence of circadian clocks and temporal control of differentiation in Anabaena filaments

Arbel-Goren,

Dassa,

Zhitnitsky

et al. 2024

mSystems

0

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Circadian clock arrays in multicellular filaments of the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 display remarkable spatio-temporal coherence under nitrogen-replete conditions. To shed light on the interplay between circadian clocks and the formation of developmental patterns, we followed the expression of a clock-controlled gene under nitrogen deprivation, at the level of individual cells. Our experiments showed that differentiation into heterocysts took place preferentially within a limited interval of the circadian clock cycle, that gene expression in different vegetative intervals along a developed filament was discoordinated, and that the circadian clock was active in individual heterocysts. Furthermore, Anabaena mutants lacking the kaiABC genes encoding the circadian clock core components produced heterocysts but failed in diazotrophy. Therefore, genes related to some aspect of nitrogen fixation, rather than early or mid-heterocyst differentiation genes, are likely affected by the absence of the clock. A bioinformatics analysis supports the notion that RpaA may play a role as master regulator of clock outputs in Anabaena , the temporal control of differentiation by the circadian clock and the involvement of the clock in proper diazotrophic growth. Together, these results suggest that under nitrogen-deficient conditions, the clock coherent unit in Anabaena is reduced from a full filament under nitrogen-rich conditions to the vegetative cell interval between heterocysts. IMPORTANCE Circadian clocks, from unicellular organisms to animals, temporally align biological processes to day and night cycles. We study the dynamics of a circadian clock-controlled gene at the individual cell level in the multicellular filamentous cyanobacterium Anabaena , under nitrogen-stress conditions. Under these conditions, some cells along filaments differentiate to carry out atmospheric nitrogen fixation and lose their capability for oxygenic photosynthesis. We found that clock synchronization is limited to organismic units of contiguous photosynthetic cells, contrary to nitrogen-replete conditions in which clocks are synchronized over a whole filament. We provided evidence that the circadian clock regulates the process of differentiation, allowing it to occur preferentially within a limited time window during the circadian clock period. Lastly, we present evidence that the signal from the core clock to clock-regulated genes is conveyed in Anabaena as in unicellular cyanobacteria.

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“…Here we found that upstream of pecB there are two putative RpaA binding sites (p value=1.5x10 -5 , Table S1). Since neither the abundance of RpaA nor its transcription decrease as a result of nitrogen deprivation (Camargo et al, 2021;Zhang et al, 2021), lower levels of pecBACEF transcription may be effected by a reduction in the levels of the active phosphorylated form (RpaA~P), which may be mediated by SasA and CikA in Anabaena as in S.…”

Section: Discussionmentioning

confidence: 99%

“…Here we found that upstream of pecB there are two putative RpaA binding sites (p value=1.5×10 -5 , Table S1). Since neither the abundance of RpaA nor its transcription decrease as a result of nitrogen deprivation (Camargo et al, 2021; Zhang et al, 2021), lower levels of pecBACEF transcription may be effected by a reduction in the levels of the active phosphorylated form (RpaA~P), which may be mediated by SasA and CikA in Anabaena as in S. elongatus (Gutu and O’Shea, 2013). SasA is regulated in S. elongatus by the phycobilisome-associated B protein (RpaB), which is involved in the integration of temporal and environmental information and stress (Espinosa et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Spatio-temporal coherence of circadian clocks and gating of differentiation inAnabaenafilaments

Arbel-Goren

¹

,

Dassa

²

,

Zhitnitsky

³

et al. 2023

Preprint

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Circadian clock arrays in multicellular filaments of the heterocyst-forming cyanobacteriumAnabaenasp. strain PCC 7120 display remarkable spatio-temporal coherence under nitrogen-replete conditions. To shed light on the interplay between circadian clocks and the formation of developmental patterns, we followed the expression of a clock-controlled gene under nitrogen deprivation, at the level of individual cells. Our experiments showed that differentiation into heterocysts took place preferentially within a limited interval of the circadian clock cycle; that gene expression in different vegetative intervals along a developed filament was discoordinated; and that the circadian clock was active in individual heterocysts. Furthermore,Anabaenamutants lacking thekaiABCgenes encoding the circadian clock core components produced heterocysts but failed in diazotrophy. Therefore, genes related to some aspect of nitrogen fixation, rather than early or mid-heterocyst differentiation genes, are likely affected by the absence of the clock. A bioinformatics analysis supports the notion that RpaA may play a role as master regulator of clock outputs inAnabaena,the gating of differentiation by the circadian clock and the involvement of the clock in proper diazotrophic growth. Together, these results suggest that under nitrogen deficient conditions, the functional unit inAnabaenais reduced from a full filament under nitrogen-rich conditions, to the vegetative cell interval between heterocysts.

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“…As cyanobacteria are exposed to dynamic environmental conditions, they have developed sophisticated defense and detoxification systems to ameliorate the consequences of stress-induced reactive oxygen species (ROS). While the dynamics of cyanobacterial intracellular processes related to stress responses has been studied intensively ( 1 – 12 ), there are significant gaps in our understanding of the stresses managed in the extracellular space. In addition to a variety of exometabolites, cyanobacterial extracellular milieu is rich in proteins, whether they are actively secreted or not ( 13 – 18 ).…”

Section: Introductionmentioning

confidence: 99%

FurC (PerR) contributes to the regulation of peptidoglycan remodeling and intercellular molecular transfer in the cyanobacterium Anabaena sp. strain PCC 7120

Sarasa-Buisan,

Nieves-Morión,

Arévalo

et al. 2024

mBio

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Cyanobacteria are ubiquitous photosynthetic prokaryotes that can adapt to environmental stresses by modulating their extracellular contents. Measurements of the organization and composition of the extracellular milieu provide useful information about cyanobacterial adaptive processes, which can potentially lead to biomimetic approaches to stabilizing biological systems to adverse conditions. Anabaena sp. strain PCC 7120 is a multicellular, nitrogen-fixing cyanobacterium whose intercellular molecular exchange is mediated by septal junctions that traverse the septal peptidoglycan through nanopores. FurC (PerR) is an essential transcriptional regulator in Anabaena , which modulates the response to several stresses. Here, we show that furC -overexpressing cells result in a modified exoproteome and the release of peptidoglycan fragments. Phenotypically, important alterations in nanopore formation and cell-to-cell communication were observed. Our results expand the roles of FurC to the modulation of cell-wall biogenesis and recycling, as well as in intercellular molecular transfer.

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Quantitative Proteomics Reveals the Protein Regulatory Network of Anabaena sp. PCC 7120 under Nitrogen Deficiency

Cited by 7 publications

References 63 publications

Spatio-temporal coherence of circadian clocks and temporal control of differentiation in Anabaena filaments

Spatio-temporal coherence of circadian clocks and temporal control of differentiation in Anabaena filaments

Spatio-temporal coherence of circadian clocks and gating of differentiation inAnabaenafilaments

FurC (PerR) contributes to the regulation of peptidoglycan remodeling and intercellular molecular transfer in the cyanobacterium Anabaena sp. strain PCC 7120

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