Interactions Between Histidine Kinase NblS and the Response Regulators RpaB and SrrA are Involved in the Bleaching Process of the Cyanobacterium Synechococcus elongatus PCC 7942

Katô, Hiroaki; Kubo, T.; Hayashi, Maiko; Kobayashi, Ikki; Yagasaki, Tatsuya; Chibazakura, Taku; Watanabe, Satoru; Yoshikawa, Hideki

doi:10.1093/pcp/pcr140

Cited by 31 publications

(26 citation statements)

References 27 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…As an HK partner of NrrA has not yet been identified, our results support the hypothesis that NrrA interacts with multiple HK partners and that integration of input signals is a component of its function in metabolic regulation. Our DCA results also agree with in vivo studies that demon- strated the HK NblS interacting with both RpaB and SrrA in a branched pathway (36,37). Identification of the core circadian oscillator.…”

Section: Resultssupporting

confidence: 89%

A Combined Computational and Genetic Approach Uncovers Network Interactions of the Cyanobacterial Circadian Clock

et al. 2016

View full text Add to dashboard Cite

Two-component systems (TCS) that employ histidine kinases (HK) and response regulators (RR) are critical mediators of cellular signaling in bacteria. In the model cyanobacterium Synechococcus elongatus PCC 7942, TCSs control global rhythms of transcription that reflect an integration of time information from the circadian clock with a variety of cellular and environmental inputs. The HK CikA and the SasA/RpaA TCS transduce time information from the circadian oscillator to modulate downstream cellular processes. Despite immense progress in understanding of the circadian clock itself, many of the connections between the clock and other cellular signaling systems have remained enigmatic. To narrow the search for additional TCS components that connect to the clock, we utilized direct-coupling analysis (DCA), a statistical analysis of covariant residues among related amino acid sequences, to infer coevolution of new and known clock TCS components. DCA revealed a high degree of interaction specificity between SasA and CikA with RpaA, as expected, but also with the phosphate-responsive response regulator SphR. Coevolutionary analysis also predicted strong specificity between RpaA and a previously undescribed kinase, HK0480 (herein CikB). A knockout of the gene for CikB (cikB) in a sasA cikA null background eliminated the RpaA phosphorylation and RpaA-controlled transcription that is otherwise present in that background and suppressed cell elongation, supporting the notion that CikB is an interactor with RpaA and the clock network. This study demonstrates the power of DCA to identify subnetworks and key interactions in signaling pathways and of combinatorial mutagenesis to explore the phenotypic consequences. Such a combined strategy is broadly applicable to other prokaryotic systems. IMPORTANCESignaling networks are complex and extensive, comprising multiple integrated pathways that respond to cellular and environmental cues. A TCS interaction model, based on DCA, independently confirmed known interactions and revealed a core set of subnetworks within the larger HK-RR set. We validated high-scoring candidate proteins via combinatorial genetics, demonstrating that DCA can be utilized to reduce the search space of complex protein networks and to infer undiscovered specific interactions for signaling proteins in vivo. Significantly, new interactions that link circadian response to cell division and fitness in a light/dark cycle were uncovered. The combined analysis also uncovered a more basic core clock, illustrating the synergy and applicability of a combined computational and genetic approach for investigating prokaryotic signaling networks. Bacterial two-component systems (TCS) are ubiquitous signaling modules consisting of at least one histidine kinase (HK) and one response regulator (RR) (1), which transduce signals via transfer of a phosphate group from the HK to a receiver domain on the RR. Over the years, studies have expanded the common paradigm of TCS signaling via phosphotransfer between single HK-RR pa...

show abstract

Section: Resultssupporting

confidence: 89%

A Combined Computational and Genetic Approach Uncovers Network Interactions of the Cyanobacterial Circadian Clock

et al. 2016

View full text Add to dashboard Cite

show abstract

“…Rather, RpaB and SrrA, response regulators of the OmpR family, were shown to interact with NblS of Synechococcus elongatus strain PCC 7942 (Kato et al, 2011). These results support negative regulation of nblA transcription under nutrient replete conditions by the NblS-RpaB pathway (Kato et al, 2011) in accordance with a previous suggestion that NblS represses nblA transcription (Kappell et al, 2006). RpaB and SrrA bind to an HLR1 element in the nblA promoter, and deletion of rpaB (but not srrA) increased nblA transcript abundance under nutrient replete conditions without affecting transcript levels in nitrogen-starved cells.…”

Section: Regulation Of Pbs Degradationmentioning

confidence: 95%

“…Rather, RpaB and SrrA, response regulators of the OmpR family, were shown to interact with NblS of Synechococcus elongatus strain PCC 7942 (Kato et al, 2011). Rather, RpaB and SrrA, response regulators of the OmpR family, were shown to interact with NblS of Synechococcus elongatus strain PCC 7942 (Kato et al, 2011).…”

Section: Regulation Of Pbs Degradationmentioning

confidence: 98%

Nitrogen chlorosis in unicellular cyanobacteria – a developmental program for surviving nitrogen deprivation

Forchhammer

Schwarz

2018

Environmental Microbiology

View full text Add to dashboard Cite

Summary Cyanobacteria evolved sophisticated mechanisms allowing them to cope with environmental depletion of combined nitrogen. Here, we describe progress in understanding the processes involved in acclimation of nondiazotrophic cyanobacteria to nitrogen shortage, known as nitrogen chlorosis. The process includes immediate metabolic changes and degradation of light harvesting complexes as well as long‐term acclimation responses. Consequently, quiescent cells substantially differing from vegetative cells are obtained. Thus, the process leading to these considerable metabolic and morphological changes is referred to as a developmental program. Current understanding of the relevant regulatory processes depicts an intricate mechanism involving modulation of transcription activators by proteinaceous interacting components, as well as by small metabolites reporting the energy status and carbon–nitrogen balance of the cell. In addition, we describe in detail the quiescent state characterizing cells under prolonged starvation and the process of recovery from this dormant chlorotic state. Accumulated data provide an in depth understanding of the mechanisms accompanying the cycling of cyanobacterial cells between vegetative growth, the quiescent‐state and the recovery program, allowing them to regain proliferative growth upon nutrient replenishment.

show abstract

“…Orthologs of NblA of S. elongatus (proteins of~6-7 kDa) have been identified in a variety of cyanobacteria and red algae (Baier et al, 2001(Baier et al, , 2004Richaud et al, 2001;Li and Sherman, 2002;Luque et al, 2003;de Alda et al, 2004;Kawakami et al, 2009). Transcription of nblA, which is induced by specific environmental cues, is subject to complex and tight regulation (Schwarz and Grossman, 1998;Sauer et al, 1999;Luque et al, 2001;van Waasbergen et al, 2002;Osanai et al, 2005;Sendersky et al, 2005;Lahmi et al, 2006;Salinas et al, 2007;Zabulon et al, 2007;Kato et al, 2008Kato et al, , 2011Ruiz et al, 2008;Leganes et al, 2009). Recently, homologs of NblA were identified in the genomes of cyanophages (Yoshida et al, 2008;Gao et al, 2012;Yoshida-Takashima et al, 2012;Nakamura et al, 2014), however, the role of these viral nblA genes in phage infection is yet unknown.…”

Section: Introductionmentioning

confidence: 99%

The proteolysis adaptor, NblA, initiates protein pigment degradation by interacting with the cyanobacterial light‐harvesting complexes

et al. 2014

View full text Add to dashboard Cite

SUMMARYDegradation of the cyanobacterial protein pigment complexes, the phycobilisomes, is a central acclimation response that controls light energy capture. The small protein, NblA, is essential for proteolysis of these large complexes, which may reach a molecular mass of up to 4 MDa. Interactions of NblA in vitro supported the suggestion that NblA is a proteolysis adaptor that labels the pigment proteins for degradation. The mode of operation of NblA in situ, however, remained unresolved. Particularly, it was unclear whether NblA interacts with phycobilisome proteins while part of the large complex, or alternatively interaction with NblA, necessitates dissociation of pigment subunits from the assembly. Fluorescence intensity profiles demonstrated the preferential presence of NblA::GFP (green fluorescent protein) at the photosynthetic membranes, indicating co-localization with phycobilisomes. Furthermore, fluorescence lifetime imaging microscopy provided in situ evidence for interaction of NblA with phycobilisome protein pigments. Additionally, we demonstrated the role of NblA in vivo as a proteolysis tag based on the rapid degradation of the fusion protein NblA::GFP compared with free GFP. Taken together, these observations demonstrated in vivo the role of NblA as a proteolysis adaptor. Additionally, the interaction of NblA with phycobilisomes indicates that the dissociation of protein pigment subunits from the large complex is not a prerequisite for interaction with this adaptor and, furthermore, implicates NblA in the disassembly of the protein pigment complex. Thus, we suggest that, in the case of proteolysis of the phycobilisome, the adaptor serves a dual function: undermining the complex stability and designating the dissociated pigments for degradation.

show abstract

Interactions Between Histidine Kinase NblS and the Response Regulators RpaB and SrrA are Involved in the Bleaching Process of the Cyanobacterium Synechococcus elongatus PCC 7942

Cited by 31 publications

References 27 publications

A Combined Computational and Genetic Approach Uncovers Network Interactions of the Cyanobacterial Circadian Clock

A Combined Computational and Genetic Approach Uncovers Network Interactions of the Cyanobacterial Circadian Clock

Nitrogen chlorosis in unicellular cyanobacteria – a developmental program for surviving nitrogen deprivation

The proteolysis adaptor, NblA, initiates protein pigment degradation by interacting with the cyanobacterial light‐harvesting complexes

Contact Info

Product

Resources

About