Molecular bases of an alternative dual-enzyme system for light color acclimation of marineSynechococcuscyanobacteria

Abstract

Marine Synechococcus cyanobacteria owe their ubiquity in part to the wide pigment diversity of their light-harvesting complexes. In open ocean waters, cells predominantly possess sophisticated antennae with rods composed of phycocyanin and two types of phycoerythrins (PEI and PEII). Some strains are specialized for harvesting either green or blue light, while others can dynamically modify their light absorption spectrum to match the dominant ambient color. This process, called type IV chromatic acclimation (CA4), has been linked to the presence of a small genomic island occurring in two configurations (CA4-A and CA4-B). While the CA4-A process has been partially characterized, the CA4-B process has remained an enigma. Here we characterize the function of two members of the phycobilin lyase E/F clan, MpeW and MpeQ, in Synechococcus sp. strain A15-62 and demonstrate their critical role in CA4-B. While MpeW, encoded in the CA4-B island and up-regulated in green light, attaches the green light-absorbing chromophore phycoerythrobilin to cysteine-83 of the PEII α-subunit in green light, MpeQ binds phycoerythrobilin and isomerizes it into the blue light-absorbing phycourobilin at the same site in blue light, reversing the relationship of MpeZ and MpeY in the CA4-A strain RS9916. Our data thus reveal key molecular differences between the two types of chromatic acclimaters, both highly abundant but occupying distinct complementary ecological niches in the ocean. They also support an evolutionary scenario whereby CA4-B island acquisition allowed former blue light specialists to become chromatic acclimaters, while former green light specialists would have acquired this capacity by gaining a CA4-A island.

Diversity and evolution of pigment types and the phycobilisome rod gene region of marine Synechococcus cyanobacteria

“…This arrangement, which has thus far only been observed in MINOS11, suggests that rpcG expression could be controlled by light color and its protein product compete with those encoded by the rpcE-F operon, since both act on the same cysteine residue of α-PC (Swanson et al 1992;Zhou et al 1992;Blot et al 2009). This arrangement would be similar to the relationship between mpeZ and mpeY (Sanfilippo, Nguyen, et al 2019) or between mpeW and mpeQ (Grébert et al 2021). If confirmed, this would be the first case of chromatic acclimation altering the chromophorylation of PC instead of PE-I and PE-II in marine Synechococcus.…”

“…S8). Such highly divergent sequences may in some cases reflect functional differences, as was recently demonstrated for MpeY and MpeQ (Grébert et al 2021) and for CpeF and MpeV .…”

“…The main difference between the PBS rod regions of PT 2A and 3a is the presence in the latter of a small cluster of five genes between cpeR and cpeY, including unk8/7, a fusion of unk8 and unk7 found as separate genes in all other PT 3 subtypes, unk9, another gene of unknown function, the recently characterized PEB lyase gene mpeY (Sanfilippo, Nguyen, et al 2019;Grébert et al 2021), and the mpeBA operon encoding the α− and β−PE-II subunits (Fig. 1 and Figs.…”

“…In contrast, the PT 3a and 3dA PBS-encoding regions differ by a number of genes and often have different alleles for orthologous genes. Thus, although the acquisition of a CA4-A island theoretically should be sufficient to transform a PT 3a-type green light specialist into a chromatic acclimater (Sanfilippo, Nguyen, et al 2019;Grébert et al 2021), the divergence between the PT 3a and 3dA PBS components could make this conversion problematic. In accordance with this, although a number of PT 3a strains have naturally acquired either a complete (MVIR-18-1) or a partial (WH8016 and KORDI-49) CA4-A genomic island (so-called PT 3aA strains), none exhibit a functional CA4 phenotype (Choi and Noh 2009;Humily et al 2013).…”

“…Moreover, the conserved hypothetical gene unk10, which is absent from all PT 3a, is present in the middle of the PBS rod region of all 3c and 3dB PTs, while in PT 3dA strains it is always located in the CA4-A island, thus outside the PBS rod region. Finally, the lyase-isomerase gene mpeQ is present in 3c and 3dB PTs instead of the lyase gene mpeY (Sanfilippo, Nguyen, et al 2019;Grébert et al 2021).…”