%0 Journal Article %J Genome Biology and Evolution %D 2022 %T Diversity and evolution of pigment types in marine \textit{Synechococcus cyanobacteria %A Grébert, Théophile %A Garczarek, Laurence %A Daubin, Vincent %A Humily, Florian %A Marie, Dominique %A Ratin, Morgane %A Devailly, Alban %A Farrant, Gregory K. %A Mary, Isabelle %A Mella-Flores, Daniella %A Tanguy, Gwenn %A Labadie, Karine %A Wincker, Patrick %A Kehoe, David M. %A Partensky, Frédéric %E Angert, Esther %K RCC307 %K to add %X DNA integration and site-specific recombination, suggesting that their genomic variability relies D in part on a ‘tycheposon’-like mechanism. Comparison of the phylogenies obtained for PBS and E core genes revealed that the evolutionary history of PBS rod genes differs from the core T genome and is characterized by the co-existence of different alleles and frequent allelic P exchange. We propose a scenario for the evolution of the different pigment types and highlight E the importance of incomplete lineage sorting in maintaining a wide diversity of pigment types in C different Synechococcus lineages despite multiple speciation events. %B Genome Biology and Evolution %P evac035 %G eng %U https://academic.oup.com/gbe/advance-article/doi/10.1093/gbe/evac035/6547267 %R 10.1093/gbe/evac035 %0 Journal Article %J mBio %D 2022 %T Multiple Photolyases Protect the Marine Cyanobacterium Synechococcus from Ultraviolet Radiation %A Haney, Allissa M. %A Sanfilippo, Joseph E. %A Garczarek, Laurence %A Partensky, Frédéric %A Kehoe, David M. %E Ruby, Edward %K rcc555 %X

Marine cyanobacteria depend on light for photosynthesis, restricting their growth to the photic zone. The upper part of this layer is exposed to strong UV radiation (UVR), a DNA mutagen that can harm these microorganisms. To thrive in UVR-rich waters, marine cyanobacteria employ photoprotection strategies that are still not well defined. Among these are photolyases, light-activated enzymes that repair DNA dimers generated by UVR. Our analysis of genomes of 81 strains of Synechococcus, Cyanobium, and Prochlorococcus isolated from the world’s oceans shows that they possess up to five genes encoding different members of the photolyase/cryptochrome family, including a photolyase with a novel domain arrangement encoded by either one or two separate genes. We disrupted the putative photolyase-encoding genes in Synechococcus sp. strain RS9916 and discovered that each gene contributes to the overall capacity of this organism to survive UVR. Additionally, each conferred increased survival after UVR exposure when transformed into Escherichia coli lacking its photolyase and SOS response. Our results provide the first evidence that this large set of photolyases endows Synechococcus with UVR resistance that is far superior to that of E. coli, but that, unlike for E. coli, these photolyases provide Synechococcus with the vast majority of its UVR tolerance.

%B mBio %V 13 %P e01511–22 %8 aug %G eng %U https://journals.asm.org/doi/10.1128/mbio.01511-22 %R 10.1128/mbio.01511-22 %0 Journal Article %J Proceedings of the National Academy of Sciences %D 2021 %T Molecular bases of an alternative dual-enzyme system for light color acclimation of marine \textit{Synechococcus cyanobacteria %A Grébert, Théophile %A Nguyen, Adam A. %A Pokhrel, Suman %A Joseph, Kes Lynn %A Ratin, Morgane %A Dufour, Louison %A Chen, Bo %A Haney, Allissa M. %A Karty, Jonathan A. %A Trinidad, Jonathan C. %A Garczarek, Laurence %A Schluchter, Wendy M. %A Kehoe, David M. %A Partensky, Frédéric %K RCC2374 %K to add %X

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.

%B Proceedings of the National Academy of Sciences %V 118 %P e2019715118 %G eng %U http://www.pnas.org/lookup/doi/10.1073/pnas.2019715118 %R 10.1073/pnas.2019715118 %0 Journal Article %J Biochimica et Biophysica Acta (BBA) - Bioenergetics %D 2020 %T CpeY is a phycoerythrobilin lyase for cysteine 82 of the phycoerythrin I α-subunit in marine Synechococcus %A Carrigee, Lyndsay A. %A Mahmoud, Rania M. %A Sanfilippo, Joseph E. %A Frick, Jacob P. %A Strnat, Johann A. %A Karty, Jonathan A. %A Chen, Bo %A Kehoe, David M. %A Schluchter, Wendy M. %K rcc555 %B Biochimica et Biophysica Acta (BBA) - Bioenergetics %P 148215 %8 apr %G eng %U https://doi.org/10.1016/j.bbamem.2019.183135 https://linkinghub.elsevier.com/retrieve/pii/S0005272820300657 %R 10.1016/j.bbabio.2020.148215 %0 Journal Article %J Proceedings of the National Academy of Sciences %D 2019 %T Interplay between differentially expressed enzymes contributes to light color acclimation in marine Synechococcus %A Sanfilippo, Joseph E. %A Nguyen, Adam A. %A Garczarek, Laurence %A Karty, Jonathan A. %A Pokhrel, Suman %A Strnat, Johann A. %A Partensky, Frédéric %A Schluchter, Wendy M. %A Kehoe, David M. %K RCC1086 %K RCC2035 %K rcc2380 %K rcc2382 %K RCC2385 %K RCC2433 %K RCC2437 %K RCC2528 %K RCC2533 %K RCC2534 %K RCC2535 %K RCC2571 %K RCC2673 %K RCC28 %K RCC307 %K RCC328 %K RCC515 %K rcc555 %K rcc791 %X Marine Synechococcus , a globally important group of cyanobacteria, thrives in various light niches in part due to its varied photosynthetic light-harvesting pigments. Many Synechococcus strains use a process known as chromatic acclimation to optimize the ratio of two chromophores, green-light–absorbing phycoerythrobilin (PEB) and blue-light–absorbing phycourobilin (PUB), within their light-harvesting complexes. A full mechanistic understanding of how Synechococcus cells tune their PEB to PUB ratio during chromatic acclimation has not yet been obtained. Here, we show that interplay between two enzymes named MpeY and MpeZ controls differential PEB and PUB covalent attachment to the same cysteine residue. MpeY attaches PEB to the light-harvesting protein MpeA in green light, while MpeZ attaches PUB to MpeA in blue light. We demonstrate that the ratio of mpeY to mpeZ mRNA determines if PEB or PUB is attached. Additionally, strains encoding only MpeY or MpeZ do not acclimate. Examination of strains of Synechococcus isolated from across the globe indicates that the interplay between MpeY and MpeZ uncovered here is a critical feature of chromatic acclimation for marine Synechococcus worldwide. %B Proceedings of the National Academy of Sciences %V 116 %P 6457–6462 %8 mar %G eng %U http://www.pnas.org/lookup/doi/10.1073/pnas.1810491116 %R 10.1073/pnas.1810491116 %0 Journal Article %J Proceedings of the National Academy of Sciences %D 2018 %T Light color acclimation is a key process in the global ocean distribution of Synechococcus cyanobacteria %A Grébert, Théophile %A Doré, Hugo %A Partensky, Frédéric %A Farrant, Gregory K. %A Boss, Emmanuel S. %A Picheral, Marc %A Guidi, Lionel %A Pesant, Stéphane %A Scanlan, David J. %A Wincker, Patrick %A Acinas, Silvia G. %A Kehoe, David M. %A Garczarek, Laurence %K 2018 %K RCC1016 %K RCC1017 %K RCC1018 %K RCC1020 %K RCC1023 %K RCC1027 %K RCC1030 %K RCC1031 %K rcc1084 %K RCC1085 %K RCC1086 %K RCC1087 %K RCC1096 %K RCC1097 %K RCC1649 %K RCC1661 %K RCC1688 %K RCC2032 %K RCC2033 %K RCC2035 %K RCC2319 %K RCC2366 %K RCC2368 %K RCC2369 %K RCC2370 %K RCC2372 %K RCC2373 %K RCC2374 %K RCC2375 %K RCC2376 %K RCC2378 %K RCC2379 %K rcc2380 %K RCC2381 %K rcc2382 %K RCC2383 %K RCC2384 %K RCC2385 %K RCC2415 %K RCC2432 %K RCC2433 %K RCC2434 %K RCC2435 %K RCC2436 %K RCC2437 %K RCC2438 %K RCC2457 %K RCC2525 %K RCC2526 %K RCC2527 %K RCC2528 %K RCC2529 %K RCC2530 %K RCC2532 %K RCC2533 %K RCC2534 %K RCC2536 %K RCC2553 %K RCC2554 %K RCC2555 %K RCC2556 %K RCC2567 %K RCC2568 %K RCC2569 %K RCC2570 %K RCC2571 %K RCC2673 %K rcc30 %K RCC3010 %K RCC3012 %K RCC3014 %K RCC307 %K RCC316 %K RCC318 %K RCC325 %K RCC326 %K RCC328 %K RCC37 %K RCC44 %K RCC46 %K RCC47 %K RCC515 %K rcc539 %K RCC542 %K RCC543 %K RCC550 %K RCC552 %K RCC553 %K rcc555 %K RCC556 %K RCC557 %K RCC558 %K RCC559 %K RCC62 %K RCC650 %K RCC66 %K rcc752 %K RCC753 %K RCC790 %K rcc791 %K RCC792 %K RCC793 %K RCC794 %K sbr?hyto?app %X Marine Synechococcus cyanobacteria are major contributors to global oceanic primary production and exhibit a unique diversity of photosynthetic pigments, allowing them to exploit a wide range of light niches. However, the relationship between pigment content and niche partitioning has remained largely undetermined so far due to the lack of a single-genetic marker resolving all pigment types (PT). Here, we developed a novel and robust method based on three distinct marker genes to estimate the relative abundance of all Synechococcus PTs from metagenomes. Analysis of the Tara Oceans dataset allowed us to unveil for the first time the global distribution of Synechococcus PTs and to decipher their realized environmental niches. Green-light specialists (PT 3a) dominated in warm, green equatorial waters, whereas blue-light specialists (PT 3c) were particularly abundant in oligotrophic areas. Type IV chromatic acclimaters (CA4-A/B), which are able to dynamically modify their light absorption properties to maximally absorb green or blue light, were unexpectedly the most abundant PT in our dataset and predominated at depth and high latitudes. We also identified local populations in which CA4 might be inactive due to the lack of specific CA4 genes, notably in warm high nutrient low chlorophyll areas. Major ecotypes within clades I-IV and CRD1 were preferentially associated with a particular PT, while others exhibited a wide range of PTs. Altogether, this study brings unprecedented insights into the ecology of Synechococcus PTs and highlights the complex interactions between vertical phylogeny, pigmentation and environmental parameters that shape Synechococcus populations and evolution. %B Proceedings of the National Academy of Sciences %V in press %P 201717069 %8 feb %G eng %U http://www.pnas.org/lookup/doi/10.1073/pnas.1717069115 %R 10.1073/pnas.1717069115 %0 Journal Article %J Frontiers in Microbiology %D 2017 %T Adaptation to blue light in marine synechococcus requires MpeU, an enzyme with similarity to phycoerythrobilin lyase isomerases %A Mahmoud, Rania M. %A Sanfilippo, Joseph E. %A Nguyen, Adam A. %A Strnat, Johann A. %A Partensky, Frédéric %A Garczarek, Laurence %A Abo El Kassem, Nabil %A Kehoe, David M. %A Schluchter, Wendy M. %K 2017 %K Blue light %K light harvesting complex %K Lyase isomerase %K marine cyanobacteria %K Marine Synechococcus %K phycobilin %K Phycobilisome %K Phycoerythrin %K Phycourobilin %K rcc555 %K sbr?hyto?app %X Marine Synechococcus cyanobacteria have successfully adapted to environments with different light colors, which likely contributes to this genus being the second most abundant photosynthetic microorganism worldwide. Populations of Synechococcus that grow in deep, blue ocean waters contain large amounts of the blue-light absorbing chromophore phycourobilin (PUB) in their light harvesting complexes (phycobilisomes). Here we show that all Synechococcus strains adapted to blue light possess a gene called mpeU. MpeU is structurally similar to phycobilin lyases, enzymes that ligate chromophores to phycobiliproteins. Interruption of mpeU caused a reduction in PUB content, produced impaired phycobilisomes and reduced growth rate more strongly in blue than green light. When mpeU was reintroduced in the mpeU mutant background, the mpeU-less phenotype was complemented in terms of PUB content and phycobilisome content. Fluorescence spectra of mpeU mutant cells and purified phycobilisomes revealed red-shifted phycoerythrin emission peaks, likely indicating a defect in chromophore ligation to phycoerythrin-I (PE-I) or phycoerythrin-II (PE-II). Our results suggest that MpeU is a lyase-isomerase that attaches a phycoerythrobilin to a PEI or PEII subunit and isomerizes it to PUB. MpeU is therefore an important determinant in adaptation of Synechococcus spp. to capture photons in blue light environments throughout the world's oceans. %B Frontiers in Microbiology %V 8 %P 243 %8 feb %G eng %U http://journal.frontiersin.org/article/10.3389/fmicb.2017.00243/full %R 10.3389/fmicb.2017.00243