Prochlorococcus and Synechococcus have Evolved Different Adaptive Mechanisms to Cope with Light and UV Stress.

International audienceProchlorococcus and Synechococcus, which numerically dominate vast oceanic areas, are the two most abundant oxygenic phototrophs on Earth. Although they require solar energy for photosynthesis, excess light and associated high UV radiations can induce high levels of oxidative stress that may have deleterious effects on their growth and productivity. Here, we compared the photophysiologies of the model strains Prochlorococcus marinus PCC 9511 and Synechococcus sp. WH7803 grown under a bell-shaped light/dark cycle of high visible light supplemented or not with UV. Prochlorococcus exhibited a higher sensitivity to photoinactivation than Synechococcus under both conditions, as shown by a larger drop of photosystem II (PSII) quantum yield at noon and different diel patterns of the D1 protein pool. In the presence of UV, the PSII repair rate was significantly depressed at noon in Prochlorococcus compared to Synechococcus. Additionally, Prochlorococcus was more sensitive than Synechococcus to oxidative stress, as shown by the different degrees of PSII photoinactivation after addition of hydrogen peroxide. A transcriptional analysis also revealed dramatic discrepancies between the two organisms in the diel expression patterns of several genes involved notably in the biosynthesis and/or repair of photosystems, light-harvesting complexes, CO(2) fixation as well as protection mechanisms against light, UV, and oxidative stress, which likely translate profound differences in their light-controlled regulation. Altogether our results suggest that while Synechococcus has developed efficient ways to cope with light and UV stress, Prochlorococcus cells seemingly survive stressful hours of the day by launching a minimal set of protection mechanisms and by temporarily bringing down several key metabolic processes. This study provides unprecedented insights into understanding the distinct depth distributions and dynamics of these two picocyanobacteria in the field

Light history influences the response of the marine cyanobacterium Synechococcus sp. WH7803 to oxidative stress.

International audienceMarine Synechococcus undergo a wide range of environmental stressors, especially high and variable irradiance, which may induce oxidative stress through the generation of reactive oxygen species (ROS). While light and ROS could act synergistically on the impairment of photosynthesis, inducing photodamage and inhibiting photosystem II repair, acclimation to high irradiance is also thought to confer resistance to other stressors. To identify the respective roles of light and ROS in the photoinhibition process and detect a possible light-driven tolerance to oxidative stress, we compared the photophysiological and transcriptomic responses of Synechococcus sp. WH7803 acclimated to low light (LL) or high light (HL) to oxidative stress, induced by hydrogen peroxide (H₂O₂) or methylviologen. While photosynthetic activity was much more affected in HL than in LL cells, only HL cells were able to recover growth and photosynthesis after the addition of 25 μM H₂O₂. Depending upon light conditions and H₂O₂ concentration, the latter oxidizing agent induced photosystem II inactivation through both direct damage to the reaction centers and inhibition of its repair cycle. Although the global transcriptome response appeared similar in LL and HL cells, some processes were specifically induced in HL cells that seemingly helped them withstand oxidative stress, including enhancement of photoprotection and ROS detoxification, repair of ROS-driven damage, and regulation of redox state. Detection of putative LexA binding sites allowed the identification of the putative LexA regulon, which was down-regulated in HL compared with LL cells but up-regulated by oxidative stress under both growth irradiances

Ultraviolet stress delays chromosome replication in light/dark synchronized cells of the marine cyanobacterium Prochlorococcus marinus PCC9511.

International audienceBACKGROUND: The marine cyanobacterium Prochlorococcus is very abundant in warm, nutrient-poor oceanic areas. The upper mixed layer of oceans is populated by high light-adapted Prochlorococcus ecotypes, which despite their tiny genome (approximately 1.7 Mb) seem to have developed efficient strategies to cope with stressful levels of photosynthetically active and ultraviolet (UV) radiation. At a molecular level, little is known yet about how such minimalist microorganisms manage to sustain high growth rates and avoid potentially detrimental, UV-induced mutations to their DNA. To address this question, we studied the cell cycle dynamics of P. marinus PCC9511 cells grown under high fluxes of visible light in the presence or absence of UV radiation. Near natural light-dark cycles of both light sources were obtained using a custom-designed illumination system (cyclostat). Expression patterns of key DNA synthesis and repair, cell division, and clock genes were analyzed in order to decipher molecular mechanisms of adaptation to UV radiation. RESULTS: The cell cycle of P. marinus PCC9511 was strongly synchronized by the day-night cycle. The most conspicuous response of cells to UV radiation was a delay in chromosome replication, with a peak of DNA synthesis shifted about 2 h into the dark period. This delay was seemingly linked to a strong downregulation of genes governing DNA replication (dnaA) and cell division (ftsZ, sepF), whereas most genes involved in DNA repair (such as recA, phrA, uvrA, ruvC, umuC) were already activated under high visible light and their expression levels were only slightly affected by additional UV exposure. CONCLUSIONS: Prochlorococcus cells modified the timing of the S phase in response to UV exposure, therefore reducing the risk that mutations would occur during this particularly sensitive stage of the cell cycle. We identified several possible explanations for the observed timeshift. Among these, the sharp decrease in transcript levels of the dnaA gene, encoding the DNA replication initiator protein, is sufficient by itself to explain this response, since DNA synthesis starts only when the cellular concentration of DnaA reaches a critical threshold. However, the observed response likely results from a more complex combination of UV-altered biological processes

Over-calcified forms of the coccolithophore Emiliania huxleyi in high-CO2 waters are not preadapted to ocean acidification

Marine multicellular organisms inhabiting waters with natural high fluctuations in pH appear more tolerant to acidification than conspecifics occurring in nearby stable waters, suggesting that environments of fluctuating pH hold genetic reservoirs for adaptation of key groups to ocean acidification (OA). The abundant and cosmopolitan calcifying phytoplankton Emiliania huxleyi exhibits a range of morphotypes with varying degrees of coccolith mineralization. We show that E. huxleyi populations in the naturally acidified upwelling waters of the eastern South Pacific, where pH drops below 7.8 as is predicted for the global surface ocean by the year 2100, are dominated by exceptionally over-calcified morphotypes whose distal coccolith shield can be almost solid calcite. Shifts in morphotype composition of E. huxleyi populations correlate with changes in carbonate system parameters. We tested if these correlations indicate that the hyper-calcified morphotype is adapted to OA. In experimental exposures to present-day vs. future pCO2 (400 vs. 1200 µatm), the over-calcified morphotypes showed the same growth inhibition (−29.1±6.3 %) as moderately calcified morphotypes isolated from non-acidified water (−30.7±8.8 %). Under the high-CO2–low-pH condition, production rates of particulate organic carbon (POC) increased, while production rates of particulate inorganic carbon (PIC) were maintained or decreased slightly (but not significantly), leading to lowered PIC ∕ POC ratios in all strains. There were no consistent correlations of response intensity with strain origin. The high-CO2–low-pH condition affected coccolith morphology equally or more strongly in over-calcified strains compared to moderately calcified strains. High-CO2–low-pH conditions appear not to directly select for exceptionally over-calcified morphotypes over other morphotypes, but perhaps indirectly by ecologically correlated factors. More generally, these results suggest that oceanic planktonic microorganisms, despite their rapid turnover and large population sizes, do not necessarily exhibit adaptations to naturally high-CO2 upwellings, and this ubiquitous coccolithophore may be near the limit of its capacity to adapt to ongoing ocean acidification

Diversité génétique et fonctionnelle des cyanobactéries picoplanctoniques marines et adaptation aux stress environnementaux

De par leur abondance et ubiquité, les picocyanobactéries marines des genres Prochlorococcus et Synechococcus jouent un rôle clé dans l écosystème marin. Afin de mieux comprendre l'influence des facteurs environnementaux sur leur répartition, la diversité génétique et fonctionnelle de ces microorganismes à été étudiée par différentes approches. Dans le premier chapitre, la distribution des principaux clades phylogénétiques de ces deux genres a été étudiée le long d'un transect en Mer Méditerranée. Cette étude a permis de mieux comprendre la structure des populations de picocyanobactéries dans cette région et de mettre en évidence sa stabilité sur une échelle de temps de 10 ans, malgré une augmentation significative des températures de surface dans le bassin Levantin. Le second chapitre a été consacré à l'étude des réponses photophysiologiques et transcriptomiques des picocyanobactéries face aux stress lumineux et oxydant. Nos résultats ont mis en évidence que Prochlorococcus et Synechococcus répondent différemment à ces stress et des éléments de réponse ont été apportés quant au rôle respectif de la lumière et du stress oxydant sur les processus de photoacclimatation. Enfin, à travers l étude des rythmes circadiens et de la production d oxygène, nous avons exploré les conséquences physiologiques de la réduction génomique chez Prochlorococcus. Ainsi, nous avons pu mettre en évidence que malgré la perte de certains gènes impliqués dans ces processus physiologiques, cet organisme semble capable de maintenir ces fonctionnalités, bien que de manière réduite par rapport à Synechococcus. Les mécanismes compensateurs impliqués et leur mode de régulation restent encore à explorer.PARIS-BIUSJ-Sci.Terre recherche (751052114) / SudocROSCOFF-Observ.Océanol. (292393008) / SudocSudocFranceF

Comparison of photosynthetic performances of marine picocyanobacteria with different configurations of the oxygen-evolving complex

This is a pre-print of an article published in Photosynthesis Research. The final authenticated version is available online at: https://doi.International audienc

Diversity and Evolution of Pigment Types in Marine Synechococcus Cyanobacteria

International audienceSynechococcus cyanobacteria are ubiquitous and abundant in the marine environment and contribute to 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 cells 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 examine the variability of gene content 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 for DNA integration and site-specific recombination, suggesting that their genomic variability relies in part 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 core 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 incomplete lineage sorting in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events