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Abstract Photosynthesis in the world’s oceans is primarily conducted by phytoplankton, microorganisms that use many different pigments for light capture. Synechococcus is a unicellular cyanobacterium estimated to be the second most abundant marine phototroph, with a global population of 7 × 1026 cells. This group’s success is partly due to the pigment diversity in their photosynthetic light harvesting antennae, which maximize photon capture for photosynthesis. Many Synechococcus isolates adjust their antennae composition in response to shifts in the blue:green ratio of ambient light. This response was named type 4 chromatic acclimation (CA4). Research has made significant progress in understanding CA4 across scales, from its global ecological importance to its molecular mechanisms. Two forms of CA4 exist, each correlated with the occurrence of one of two distinct but related genomic islands. Several genes in these islands are differentially transcribed by the ambient blue:green light ratio. The encoded proteins control the addition of different pigments to the antennae proteins in blue versus green light, altering their absorption characteristics to maximize photon capture. These genes are regulated by several putative transcription factors also encoded in the genomic islands. Ecologically, CA4 is the most abundant of marine Synechococcus pigment types, occurring in over 40% of the population oceanwide. It predominates at higher latitudes and at depth, suggesting that CA4 is most beneficial under sub-saturating photosynthetic light irradiances. Future CA4 research will further clarify the ecological role of CA4 and the molecular mechanisms controlling this globally important form of phenotypic plasticity.more » « less
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null (Ed.)Synechococcus picocyanobacteria are ubiquitous and abundant photosynthetic organisms in the marine environment and contribute for an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon, based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examined the variability of gene sequences and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements including tyrosine recombinases, suggesting that their genomic plasticity relies on a tycheposon-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the rest of the genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of population-scale mechanisms in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events.more » « less
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MarineSynechococcuscyanobacteria 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, inSynechococcussp. 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.more » « less
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