Light‐induced alteration of c‐di‐GMP level controls motility of Synechocystis sp. PCC 6803

Abstract

SummaryCph2 from the cyanobacterium Synechocystis sp. PCC 6803 is a hybrid photoreceptor that comprises an N-terminal module for red/far-red light reception and a C-terminal module switching between a blue-and a green-receptive state. This unusual photoreceptor exerts complex, light quality-dependent control of the motility of Synechocystis sp. PCC 6803 cells by inhibiting phototaxis towards blue light. Cph2 perceives blue light by its third GAF domain that bears all characteristics of a cyanobacteriochrome (CBCR) including photoconversion between green-and blueabsorbing states as well as formation of a bilin species simultaneously tethered to two cysteines, C994 and C1022. Upon blue light illumination the CBCR domain activates the subsequent C-terminal GGDEF domain, which catalyses formation of the second messenger c-di-GMP. Accordingly, expression of the CBCR-GGDEF module in Dcph2 mutant cells restores the blue light-dependent inhibition of motility. Additional expression of the N-terminal Cph2 fragment harbouring a red/far-red interconverting phytochrome fused to a c-di-GMP degrading EAL domain restores the complex behaviour of the intact Cph2 photosensor. c-di-GMP was shown to regulate flagellar and pilibased motility in several bacteria. Here we provide the first evidence that this universal bacterial second messenger is directly involved in the light-dependent regulation of cyanobacterial phototaxis.

Structure of the Cyanobacterial Phytochrome 2 Photosensor Implies a Tryptophan Switch for Phytochrome Signaling

“…3A). In this interface, the amphiphilic ␣ 1 -helix makes first several polar interactions via its residues Arg 5 , Lys 17 PAS-less phytochromes like SynCph2(1-2) depends on their N-terminal helix.…”

“…1A) harbors not only at its N terminus the red/far-red sensitive tandem-GAF module (SynCph2(1-2) (10)) that precedes a GGDEF*-EAL effector module, but also CBCR and catalytically active GGDEF domains. This C-terminal CBCR-GGDEF module is capable of switching between blue and green light sensitive states and controls the catalytic activity of the GGDEF domain, thereby inhibiting motility by increasing c-di-GMP levels (17). The GGDEF*-EAL module likely acts as c-di-GMP degrading phosphodiesterase, as its EAL domain is catalytically active, whereas the apparently inactive GGDEF* domain is predicted to act as an allosteric, c-di-GMP-dependent regulator.…”

“…Interestingly, the founding member of the Cph2 subfamily, SynCph2, is a bimodular photoreceptor (15, 16) (molecular mass 144.7 kDa) that functions as a light-dependent master regulator for cyanobacterial motility by controlling cytosolic levels of the eubacterial second messenger c-di-GMP (17). c-di-GMP is known to be a universal regulator for pili-based motility in eubacteria (18) with domains of the GGDEF and EAL type being responsible for its synthesis and degradation (19).…”

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

“…During complementary chromatic acclimation, certain cyanobacteria alter their antenna pigment and protein compositions in response to the ambient red/green-light ratio (2,3). The ability of cyanobacteria to move toward or away from light (phototaxis) is also a light color-dependent process and is usually controlled by UV/blue-or green/red-light exposure (4)(5)(6)(7). Conversely, to date, cell aggregation has been shown to be dependent on only blue-light exposure (8).…”

Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle

“…Physiologically, CBCRs are implicated in regulation of phototaxis (30)(31)(32)(33)(34), but the best-understood CBCR function is the regulation of complementary chromatic acclimation (CCA). In CCA, cyanobacteria optimize the composition of their photosynthetic pigments in response to the availability of green and red light (35).…”