Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation

Gen Enomoto, Ni-Ni-Win, Rei Narikawa, Masahiko Ikeuchi

Research output: Contribution to journalArticle

38 Citations (Scopus)

Abstract

Cyanobacteriochromes (CBCRs) are cyanobacterial photoreceptors that have diverse spectral properties and domain compositions. Although large numbers of CBCR genes exist in cyanobacterial genomes, no studies have assessed whether multiple CBCRs work together. We recently showed that the diguanylate cyclase (DGC) activity of the CBCR SesA from Thermosynechococcus elongatus is activated by blue-light irradiation and that, when irradiated, SesA, via its product cyclic dimeric GMP (c-di-GMP), induces aggregation of Thermosynechococcus vulcanus cells at a temperature that is suboptimum for single-cell viability. For this report, we first characterize the photobiochemical properties of two additional CBCRs, SesB and SesC. Blue/teal light-responsive SesB has only c-di-GMP phosphodiesterase (PDE) activity, which is up-regulated by teal light and GTP. Blue/green light-responsive SesC has DGC and PDE activities. Its DGC activity is enhanced by blue light, whereas its PDE activity is enhanced by green light. A ΔsesB mutant cannot suppress cell aggregation under teal-green light. A ΔsesC mutant shows a less sensitive cell-aggregation response to ambient light. ΔsesA/ΔsesB/ΔsesC shows partial cell aggregation, which is accompanied by the loss of color dependency, implying that a nonphotoresponsive DGC(s) producing c-di-GMP can also induce the aggregation. The results suggest that SesB enhances the light color dependency of cell aggregation by degrading c-di-GMP, is particularly effective under teal light, and, therefore, seems to counteract the induction of cell aggregation by SesA. In addition, SesC seems to improve signaling specificity as an auxiliary backup to SesA/SesB activities. The coordinated action of these three CBCRs highlights why so many different CBCRs exist.

Original languageEnglish
Pages (from-to)8082-8087
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number26
DOIs
Publication statusPublished - Jun 30 2015
Externally publishedYes

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Cell Aggregation
Cyclic GMP
Color
Light
Methyl Green
Phosphoric Diester Hydrolases
Guanosine Triphosphate
Cell Survival
Genome
Temperature
diguanylate cyclase
Genes

All Science Journal Classification (ASJC) codes

  • General

Cite this

Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation. / Enomoto, Gen; Ni-Ni-Win; Narikawa, Rei; Ikeuchi, Masahiko.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 26, 30.06.2015, p. 8082-8087.

Research output: Contribution to journalArticle

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