title: Self-regulating genomic island encoding tandem regulators confers chromatic acclimation to marine Synechococcus.
abstract: The evolutionary success of marine Synechococcus, the second-most abundant phototrophic group in the marine environment, is partly attributable to this group's ability to use the entire visible spectrum of light for photosynthesis. This group possesses a remarkable diversity of light-harvesting pigments, and most of the group's members are orange and pink because of their use of phycourobilin and phycoerythrobilin chromophores, which are attached to antennae proteins called phycoerythrins. Many strains can alter phycoerythrin chromophore ratios to optimize photon capture in changing blue-green environments using type IV chromatic acclimation (CA4). Although CA4 is common in most marine Synechococcus lineages, the regulation of this process remains unexplored. Here, we show that a widely distributed genomic island encoding tandem master regulators named FciA (for type four chromatic acclimation island) and FciB plays a central role in controlling CA4. FciA and FciB have diametric effects on CA4. Interruption of fciA causes a constitutive green light phenotype, and interruption of fciB causes a constitutive blue light phenotype. These proteins regulate all of the molecular responses occurring during CA4, and the proteins' activity is apparently regulated posttranscriptionally, although their cellular ratio appears to be critical for establishing the set point for the blue-green switch in ecologically relevant light environments. Surprisingly, FciA and FciB coregulate only three genes within the Synechococcus genome, all located within the same genomic island as fciA and fciB These findings, along with the widespread distribution of strains possessing this island, suggest that horizontal transfer of a small, self-regulating DNA region has conferred CA4 capability to marine Synechococcus throughout many oceanic areas.
authors.affiliation: Department of Biology, Indiana University, Bloomington, IN 47405;
authors.forename: Joseph E
authors.initials: JE
authors.lastname: Sanfilippo
authors.affiliation: Department of Biological Sciences, University of New Orleans, New Orleans, LA 70148; Department of Chemistry, University of New Orleans, New Orleans, LA 70148;
authors.forename: Adam A
authors.initials: AA
authors.lastname: Nguyen
authors.affiliation: Mass Spectrometry Facility, Department of Chemistry, Indiana University, Bloomington, IN 47405;
authors.forename: Jonathan A
authors.initials: JA
authors.lastname: Karty
authors.affiliation: Department of Biology, Indiana University, Bloomington, IN 47405;
authors.forename: Animesh
authors.initials: A
authors.lastname: Shukla
authors.affiliation: Department of Biological Sciences, University of New Orleans, New Orleans, LA 70148; Department of Chemistry, University of New Orleans, New Orleans, LA 70148;
authors.forename: Wendy M
authors.initials: WM
authors.lastname: Schluchter
authors.affiliation: Sorbonne Universités, Université Pierre et Marie Curie University Paris 06, CNRS, UMR 7144, Station Biologique, Plankton Group, 29688 Roscoff, France;
authors.forename: Laurence
authors.initials: L
authors.lastname: Garczarek
authors.affiliation: Sorbonne Universités, Université Pierre et Marie Curie University Paris 06, CNRS, UMR 7144, Station Biologique, Plankton Group, 29688 Roscoff, France;
authors.forename: Frédéric
authors.initials: F
authors.lastname: Partensky
authors.affiliation: Department of Biology, Indiana University, Bloomington, IN 47405; Indiana Molecular Biology Institute, Indiana University, Bloomington, IN 47405 dkehoe@indiana.edu.
authors.forename: David M
authors.initials: DM
authors.lastname: Kehoe
mesh_terms: D000064:Acclimatization / Q000502:physiology*; D059001:Aquatic Organisms / Q000235:genetics / Q000378:metabolism; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D044404:Genomic Islands; D010799:Phycoerythrin / Q000235:genetics / Q000378:metabolism; D046940:Synechococcus / Q000235:genetics / Q000378:metabolism
chemical_list: D001426:Bacterial Proteins; D010799:Phycoerythrin
keywords: horizontal gene transfer; light regulation; marine biology; marine cyanobacteria; phycobilisome