Phycoerythrin-specific bilin lyase–isomerase controls blue-green chromatic acclimation in marineSynechococcus

Abstract

The marine cyanobacterium Synechococcus is the second most abundant phytoplanktonic organism in the world's oceans. The ubiquity of this genus is in large part due to its use of a diverse set of photosynthetic light-harvesting pigments called phycobiliproteins, which allow it to efficiently exploit a wide range of light colors. Here we uncover a pivotal molecular mechanism underpinning a widespread response among marine Synechococcus cells known as "type IV chromatic acclimation" (CA4). During this process, the pigmentation of the two main phycobiliproteins of this organism, phycoerythrins I and II, is reversibly modified to match changes in the ambient light color so as to maximize photon capture for photosynthesis. CA4 involves the replacement of three molecules of the green light-absorbing chromophore phycoerythrobilin with an equivalent number of the blue light-absorbing chromophore phycourobilin when cells are shifted from green to blue light, and the reverse after a shift from blue to green light. We have identified and characterized MpeZ, an enzyme critical for CA4 in marine Synechococcus. MpeZ attaches phycoerythrobilin to cysteine-83 of the α-subunit of phycoerythrin II and isomerizes it to phycourobilin. mpeZ RNA is six times more abundant in blue light, suggesting that its proper regulation is critical for CA4. Furthermore, mpeZ mutants fail to normally acclimate in blue light. These findings provide insights into the molecular mechanisms controlling an ecologically important photosynthetic process and identify a unique class of phycoerythrin lyase/isomerases, which will further expand the already widespread use of phycoerythrin in biotechnology and cell biology applications.light regulation | marine cyanobacteria | phycobilisomes | fluorescence | liquid chromatography-mass spectrometry

Self-regulating genomic island encoding tandem regulators confers chromatic acclimation to marine Synechococcus

“…RS9916 (hereafter 9916) as a CA4 model organism, we discovered that CA4-mediated chromophorylation changes occur at cysteines 83 (C83) and C140 within α-PEII (MpeA) and C139 within α-PEI (CpeA) (9). We also identified, within the CA4 genomic island, a gene encoding a lyase/ isomerase called MpeZ that contributes to the CA4 response by attaching PUB to C83 within MpeA in blue light.…”

“…Some marine Synechococcus strains are blue light specialists (high PUB content) or green light specialists (high PEB content), whereas other strains are capable of changing the PUB:PEB ratio within their phycobilisomes in response to changes in the ambient blue:green light ratio through a process known as type IV chromatic acclimation (hereafter called CA4) (2,(7)(8)(9). Synechococcus capable of CA4 increase the amount of PUB per phycobilisome in blue light and increase the amount of PEB per phycobilisome in green light.…”

Insights into the Biosynthesis and Assembly of Cryptophycean Phycobiliproteins

“…PBP lyases are distinguishable in the clades of E/F-, S/U-, and T-type lyases, and some members of the E/F-type have an additional isomerase function (25)(26)(27).…”

Structure and Mechanism of the Phycobiliprotein Lyase CpcT

“…Last, but not least, it should be noted that deprotonation of the cationic acylimmonium intermediate (Fig. 11) at C2 rather than C5 would result in the conversion of PCB to a phycoviolobilin chromophore; such isomerization occurs in E/F-type lyases (15,16,67) as well as in several cyanobacteriochromes during autocatalytic chromophore attachment (68 -70).…”

“…They are thought to act like chaperones or protective carriers for labile bilin chromophores (6,13,14), but additional functions have been found (15)(16)(17). E/F-type lyases are specific for attaching phycocyanobilin (PCB) to a conserved cysteine (Cys-␣84) in ␣-subunits of phycocyanin (CPC) and phycoerythrocyanin (18,19); homologous CpeY/Z catalyze addition of phycoerythrobilin to the equivalent site in phycoerythrin (20).…”