Differential acclimation kinetics of the two forms of type IV chromatic acclimaters occurring in marine Synechococcus cyanobacteria.

Synechococcus, the second most abundant marine phytoplanktonic organism, displays the widest variety of pigment content of all marine oxyphototrophs, explaining its ability to colonize all spectral niches occurring in the upper lit layer of oceans. Seven Synechococcus pigment types (PTs) have been described so far based on the phycobiliprotein composition and chromophorylation of their light-harvesting complexes, called phycobilisomes. The most elaborate and abundant PT (3d) in the open ocean consists of cells capable of type IV chromatic acclimation (CA4), i.e., to reversibly modify the ratio of the blue light-absorbing phycourobilin (PUB) to the green light-absorbing phycoerythrobilin (PEB) in phycobilisome rods to match the ambient light color. Two genetically distinct types of chromatic acclimaters, so-called PTs 3dA and 3dB, occur at similar global abundance in the ocean, but the precise physiological differences between these two types and the reasons for their complementary niche partitioning in the field remain obscure. Here, photoacclimation experiments in different mixes of blue and green light of representatives of these two PTs demonstrated that they differ by the ratio of blue-to-green light required to trigger the CA4 process. Furthermore, shift experiments between 100% blue and 100% green light, and vice-versa, revealed significant discrepancies between the acclimation pace of the two types of chromatic acclimaters. This study provides novel insights into the finely tuned adaptation mechanisms used by Synechococcus cells to colonize the whole underwater light field.

Transcriptional Mechanisms of Thermal Acclimation in Prochlorococcus.

Low temperature limits the growth and the distribution of the key oceanic primary producer Prochlorococcus, which does not proliferate above a latitude of ca. 40°. Yet, the molecular basis of thermal acclimation in this cyanobacterium remains unexplored. We analyzed the transcriptional response of the Prochlorococcus marinus strain MIT9301 in long-term acclimations and in natural Prochlorococcus populations along a temperature range enabling its growth (17 to 30°C). MIT9301 upregulated mechanisms of the global stress response at the temperature minimum (17°C) but maintained the expression levels of genes involved in essential metabolic pathways (e.g., ATP synthesis and carbon fixation) along the whole thermal niche. Notably, the declining growth of MIT9301 from the optimum to the minimum temperature was coincident with a transcriptional suppression of the photosynthetic apparatus and a dampening of its circadian expression patterns, indicating a loss in their regulatory capacity under cold conditions. Under warm conditions, the cellular transcript inventory of MIT9301 was strongly streamlined, which may also induce regulatory imbalances due to stochasticity in gene expression. The daytime transcriptional suppression of photosynthetic genes at low temperature was also observed in metatranscriptomic reads mapping to MIT9301 across the global ocean, implying that this molecular mechanism may be associated with the restricted distribution of Prochlorococcus to temperate zones. IMPORTANCE Prochlorococcus is a major marine primary producer with a global impact on atmospheric CO2 fixation. This cyanobacterium is widely distributed across the temperate ocean, but virtually absent at latitudes above 40° for yet unknown reasons. Temperature has been suggested as a major limiting factor, but the exact mechanisms behind Prochlorococcus thermal growth restriction remain unexplored. This study brings us closer to understanding how Prochlorococcus functions under challenging temperature conditions, by focusing on its transcriptional response after long-term acclimation from its optimum to its thermal thresholds. Our results show that the drop in Prochlorococcus growth rate under cold conditions was paralleled by a transcriptional suppression of the photosynthetic machinery during daytime and a loss in the organism's regulatory capacity to maintain circadian expression patterns. Notably, warm temperature induced a marked shrinkage of the organism's cellular transcript inventory, which may also induce regulatory imbalances in the future functioning of this cyanobacterium.

Nested PCR Approach for petB Gene Metabarcoding of Marine Synechococcus Populations.

The molecular diversity of marine picocyanobacterial populations, an important component of phytoplankton communities, is better characterized using high-resolution marker genes than the 16S rRNA gene as they have greater sequence divergence to differentiate between closely related picocyanobacteria groups. Although specific ribosomal primers have been developed, another general disadvantage of bacterial ribosome-based diversity analyses is the variable number of rRNA gene copies. To overcome these issues, the single-copy petB gene, encoding the cytochrome b6 subunit of the cytochrome b6f complex, has been used as a high-resolution marker gene to characterize Synechococcus diversity. We have designed new primers targeting the petB gene and proposed a nested PCR method (termed Ong_2022) for metabarcoding of marine Synechococcus populations obtained by flow cytometry cell sorting. We evaluated the specificity and sensitivity of Ong_2022 against the standard amplification protocol (termed Mazard_2012) using filtered seawater samples. The Ong_2022 approach was also tested on flow cytometry-sorted Synechococcus populations. Samples (filtered and sorted) were obtained in the Southwest Pacific Ocean, from subtropical (ST) and subantarctic (SA) water masses. The two PCR approaches using filtered samples recovered the same dominant subclades, Ia, Ib, IVa, and IVb, with small differences in relative abundance across the distinct samples. For example, subclade IVa was dominant in ST samples with the Mazard_2012 approach, while the same samples processed with Ong_2022 showed similar contributions of subclades IVa and Ib to the total community. The Ong_2022 approach generally captured a higher genetic diversity of Synechococcus subcluster 5.1 than the Mazard_2012 approach while having a lower proportion of incorrectly assigned amplicon sequence variants (ASVs). All flow cytometry-sorted Synechococcus samples could be amplified only by our nested approach. The taxonomic diversity obtained with our primers on both sample types was in agreement with the clade distribution observed by previous studies that applied other marker genes or PCR-free metagenomic approaches under similar environmental conditions. IMPORTANCE The petB gene has been proposed as a high-resolution marker gene to access the diversity of marine Synechococcus populations. A systematic metabarcoding approach based on the petB gene would improve the characterization/assessment of the Synechococcus community structure in marine planktonic ecosystems. We have designed and tested specific primers to be applied in a nested PCR protocol (Ong_2022) for metabarcoding the petB gene. The Ong_2022 protocol can be applied to samples with low DNA content, such as those obtained by flow cytometry cell sorting, allowing the simultaneous assessment of the genetic diversity of Synechococcus populations and cellular properties and activities (e.g., nutrient cell ratios or carbon uptake rates). Our approach will allow future studies using flow cytometry to investigate the link between ecological traits and taxonomic diversity of marine Synechococcus.

Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies.

The ever-increasing number of available microbial genomes and metagenomes provides new opportunities to investigate the links between niche partitioning and genome evolution in the ocean, especially for the abundant and ubiquitous marine picocyanobacteria Prochlorococcus and Synechococcus. Here, by combining metagenome analyses of the Tara Oceans dataset with comparative genomics, including phyletic patterns and genomic context of individual genes from 256 reference genomes, we show that picocyanobacterial communities thriving in different niches possess distinct gene repertoires. We also identify clusters of adjacent genes that display specific distribution patterns in the field (eCAGs) and are thus potentially involved in the same metabolic pathway and may have a key role in niche adaptation. Several eCAGs are likely involved in the uptake or incorporation of complex organic forms of nutrients, such as guanidine, cyanate, cyanide, pyrimidine, or phosphonates, which might be either directly used by cells, for example for the biosynthesis of proteins or DNA, or degraded to inorganic nitrogen and/or phosphorus forms. We also highlight the enrichment of eCAGs involved in polysaccharide capsule biosynthesis in Synechococcus populations thriving in both nitrogen- and phosphorus-depleted areas vs. low-iron (Fe) regions, suggesting that the complexes they encode may be too energy-consuming for picocyanobacteria thriving in the latter areas. In contrast, Prochlorococcus populations thriving in Fe-depleted areas specifically possess an alternative respiratory terminal oxidase, potentially involved in the reduction of Fe(III) to Fe(II). Altogether, this study provides insights into how phytoplankton communities populate oceanic ecosystems, which is relevant to understanding their capacity to respond to ongoing climate change.

Diazotrophs are overlooked contributors to carbon and nitrogen export to the deep ocean.

Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans, thereby regulating marine productivity. Yet, the group-specific contribution of diazotrophs to organic matter export has not been quantified, which so far has impeded an accurate assessment of their impact on the biological carbon pump. Here, we examine the fate of five groups of globally-distributed diazotrophs by using an original combination of mesopelagic particle sampling devices across the subtropical South Pacific Ocean. We demonstrate that cyanobacterial and non-cyanobacterial diazotrophs are exported down to 1000 m depth. Surprisingly, group-specific export turnover rates point to a more efficient export of small unicellular cyanobacterial diazotrophs (UCYN) relative to the larger and filamentous Trichodesmium. Phycoerythrin-containing UCYN-B and UCYN-C-like cells were recurrently found embedded in large (>50 µm) organic aggregates or organized into clusters of tens to hundreds of cells linked by an extracellular matrix, presumably facilitating their export. Beyond the South Pacific, our data are supported by analysis of the Tara Oceans metagenomes collected in other ocean basins, extending the scope of our results globally. We show that, when diazotrophs are found in the euphotic zone, they are also systematically present in mesopelagic waters, suggesting their transport to the deep ocean. We thus conclude that diazotrophs are a significant part of the carbon sequestered in the deep ocean and, therefore, they need to be accounted in regional and global estimates of export.

Global Phylogeography of Marine Synechococcus in Coastal Areas Reveals Strong Community Shifts.

Marine Synechococcus comprise a numerically and ecologically prominent phytoplankton group, playing a major role in both carbon cycling and trophic networks in all oceanic regions except in the polar oceans. Despite their high abundance in coastal areas, our knowledge of Synechococcus communities in these environments is based on only a few local studies. Here, we use the global metagenome data set of the Ocean Sampling Day (June 21st, 2014) to get a snapshot of the taxonomic composition of coastal Synechococcus communities worldwide, by recruitment on a reference database of 141 picocyanobacterial genomes, representative of the whole Prochlorococcus, Synechococcus, and Cyanobium diversity. This allowed us to unravel drastic community shifts over small to medium scale gradients of environmental factors, in particular along European coasts. The combined analysis of the phylogeography of natural populations and the thermophysiological characterization of eight strains, representative of the four major Synechococcus lineages (clades I to IV), also brought novel insights about the differential niche partitioning of clades I and IV, which most often co-dominate the Synechococcus community in cold and temperate coastal areas. Altogether, this study reveals several important characteristics and specificities of the coastal communities of Synechococcus worldwide. IMPORTANCE Synechococcus is the second most abundant phytoplanktonic organism on Earth, and its wide genetic diversity allowed it to colonize all the oceans except for polar waters, with different clades colonizing distinct oceanic niches. In recent years, the use of global metagenomics data sets has greatly improved our knowledge of "who is where" by describing the distribution of Synechococcus clades or ecotypes in the open ocean. However, little is known about the global distribution of Synechococcus ecotypes in coastal areas, where Synechococcus is often the dominant phytoplanktonic organism. Here, we leverage the global Ocean Sampling Day metagenomics data set to describe Synechococcus community composition in coastal areas worldwide, revealing striking community shifts, in particular along the coasts of Europe. As temperature appears as an important driver of the community composition, we also characterize the thermal preferenda of 8 Synechococcus strains, bringing new insights into the adaptation to temperature of the dominant Synechococcus clades.

Multiple Photolyases Protect the Marine Cyanobacterium Synechococcus from Ultraviolet Radiation.

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. IMPORTANCE Cells use DNA photolyases to protect their DNA from the damaging effects of UV radiation. Marine cyanobacteria possess many genes that appear to encode photolyases, but the function of the proteins encoded by these genes is unclear. The study uses comparative genomics and molecular genetic approaches to describe and characterize the roles of these proteins in DNA damage repair in the marine cyanobacterium Synechococcus. This study identifies the important role of DNA photolyases in DNA repair for these cells and describes a previously undescribed structural class of DNA of these enzymes.

Comparative Thermophysiology of Marine Synechococcus CRD1 Strains Isolated From Different Thermal Niches in Iron-Depleted Areas.

Marine Synechococcus cyanobacteria are ubiquitous in the ocean, a feature likely related to their extensive genetic diversity. Amongst the major lineages, clades I and IV preferentially thrive in temperate and cold, nutrient-rich waters, whilst clades II and III prefer warm, nitrogen or phosphorus-depleted waters. The existence of such cold (I/IV) and warm (II/III) thermotypes is corroborated by physiological characterization of representative strains. A fifth clade, CRD1, was recently shown to dominate the Synechococcus community in iron-depleted areas of the world ocean and to encompass three distinct ecologically significant taxonomic units (ESTUs CRD1A-C) occupying different thermal niches, suggesting that distinct thermotypes could also occur within this clade. Here, using comparative thermophysiology of strains representative of these three CRD1 ESTUs we show that the CRD1A strain MITS9220 is a warm thermotype, the CRD1B strain BIOS-U3-1 a cold temperate thermotype, and the CRD1C strain BIOS-E4-1 a warm temperate stenotherm. Curiously, the CRD1B thermotype lacks traits and/or genomic features typical of cold thermotypes. In contrast, we found specific physiological traits of the CRD1 strains compared to their clade I, II, III, and IV counterparts, including a lower growth rate and photosystem II maximal quantum yield at most temperatures and a higher turnover rate of the D1 protein. Together, our data suggests that the CRD1 clade prioritizes adaptation to low-iron conditions over temperature adaptation, even though the occurrence of several CRD1 thermotypes likely explains why the CRD1 clade as a whole occupies most iron-limited waters.

Diversity and Evolution of Pigment Types in Marine Synechococcus Cyanobacteria.

Synechococcus 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.

Molecular bases of an alternative dual-enzyme system for light color acclimation of marine Synechococcus cyanobacteria.

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.

Vibrational modes of water predict spectral niches for photosynthesis in lakes and oceans.

Stretching and bending vibrations of water molecules absorb photons of specific wavelengths, a phenomenon that constrains light energy available for aquatic photosynthesis. Previous work suggested that these absorption properties of water create a series of spectral niches but the theory was still too simplified to enable prediction of the spectral niches in real aquatic ecosystems. Here, we show with a state-of-the-art radiative transfer model that the vibrational modes of the water molecule delineate five spectral niches, in the violet, blue, green, orange and red parts of the spectrum. These five niches are effectively captured by chlorophylls and phycobilin pigments of cyanobacteria and their eukaryotic descendants. Global distributions of the spectral niches are predicted by satellite remote sensing and validated with observed large-scale distribution patterns of cyanobacterial pigment types. Our findings provide an elegant explanation for the biogeographical distributions of photosynthetic pigments across the lakes and oceans of our planet.

MpeV is a lyase isomerase that ligates a doubly linked phycourobilin on the ß-subunit of phycoerythrin I and II in marine Synechococcus.

Synechococcus cyanobacteria are widespread in the marine environment, as the extensive pigment diversity within their light-harvesting phycobilisomes enables them to utilize various wavelengths of light for photosynthesis. The phycobilisomes of Synechococcus sp. RS9916 contain two forms of the protein phycoerythrin (PEI and PEII), each binding two chromophores, green-light absorbing phycoerythrobilin and blue-light absorbing phycourobilin. These chromophores are ligated to specific cysteines via bilin lyases, and some of these enzymes, called lyase isomerases, attach phycoerythrobilin and simultaneously isomerize it to phycourobilin. MpeV is a putative lyase isomerase whose role in PEI and PEII biosynthesis is not clear. We examined MpeV in RS9916 using recombinant protein expression, absorbance spectroscopy, and tandem mass spectrometry. Our results show that MpeV is the lyase isomerase that covalently attaches a doubly linked phycourobilin to two cysteine residues (C50, C61) on the ß-subunit of both PEI (CpeB) and PEII (MpeB). MpeV activity requires that CpeB or MpeB is first chromophorylated by the lyase CpeS (which adds phycoerythrobilin to C82). Its activity is further enhanced by CpeZ (a homolog of a chaperone-like protein first characterized in Fremyella diplosiphon). MpeV showed no detectable activity on the α-subunits of PEI or PEII. The mechanism by which MpeV links the A and D rings of phycourobilin to C50 and C61 of CpeB was also explored using site-directed mutants, revealing that linkage at the A ring to C50 is a critical step in chromophore attachment, isomerization, and stability. These data provide novel insights into ß-PE biosynthesis and advance our understanding of the mechanisms guiding lyase isomerases.

Cyanorak v2.1: a scalable information system dedicated to the visualization and expert curation of marine and brackish picocyanobacteria genomes.

Cyanorak v2.1 (http://www.sb-roscoff.fr/cyanorak) is an information system dedicated to visualizing, comparing and curating the genomes of Prochlorococcus, Synechococcus and Cyanobium, the most abundant photosynthetic microorganisms on Earth. The database encompasses sequences from 97 genomes, covering most of the wide genetic diversity known so far within these groups, and which were split into 25,834 clusters of likely orthologous groups (CLOGs). The user interface gives access to genomic characteristics, accession numbers as well as an interactive map showing strain isolation sites. The main entry to the database is through search for a term (gene name, product, etc.), resulting in a list of CLOGs and individual genes. Each CLOG benefits from a rich functional annotation including EggNOG, EC/K numbers, GO terms, TIGR Roles, custom-designed Cyanorak Roles as well as several protein motif predictions. Cyanorak also displays a phyletic profile, indicating the genotype and pigment type for each CLOG, and a genome viewer (Jbrowse) to visualize additional data on each genome such as predicted operons, genomic islands or transcriptomic data, when available. This information system also includes a BLAST search tool, comparative genomic context as well as various data export options. Altogether, Cyanorak v2.1 constitutes an invaluable, scalable tool for comparative genomics of ecologically relevant marine microorganisms.

Evolutionary Mechanisms of Long-Term Genome Diversification Associated With Niche Partitioning in Marine Picocyanobacteria.

Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant photosynthetic organisms on Earth, an ecological success thought to be linked to the differential partitioning of distinct ecotypes into specific ecological niches. However, the underlying processes that governed the diversification of these microorganisms and the appearance of niche-related phenotypic traits are just starting to be elucidated. Here, by comparing 81 genomes, including 34 new Synechococcus, we explored the evolutionary processes that shaped the genomic diversity of picocyanobacteria. Time-calibration of a core-protein tree showed that gene gain/loss occurred at an unexpectedly low rate between the different lineages, with for instance 5.6 genes gained per million years (My) for the major Synechococcus lineage (sub-cluster 5.1), among which only 0.71/My have been fixed in the long term. Gene content comparisons revealed a number of candidates involved in nutrient adaptation, a large proportion of which are located in genomic islands shared between either closely or more distantly related strains, as identified using an original network construction approach. Interestingly, strains representative of the different ecotypes co-occurring in phosphorus-depleted waters (Synechococcus clades III, WPC1, and sub-cluster 5.3) were shown to display different adaptation strategies to this limitation. In contrast, we found few genes potentially involved in adaptation to temperature when comparing cold and warm thermotypes. Indeed, comparison of core protein sequences highlighted variants specific to cold thermotypes, notably involved in carotenoid biosynthesis and the oxidative stress response, revealing that long-term adaptation to thermal niches relies on amino acid substitutions rather than on gene content variation. Altogether, this study not only deciphers the respective roles of gene gains/losses and sequence variation but also uncovers numerous gene candidates likely involved in niche partitioning of two key members of the marine phytoplankton.

Changes in Population Age-Structure Obscure the Temperature-Size Rule in Marine Cyanobacteria.

The temperature-size Rule (TSR) states that there is a negative relationship between ambient temperature and body size. This rule has been independently evaluated for different phases of the life cycle in multicellular eukaryotes, but mostly for the average population in unicellular organisms. We acclimated two model marine cyanobacterial strains (Prochlorococcus marinus MIT9301 and Synechococcus sp. RS9907) to a gradient of temperatures and measured the changes in population age-structure and cell size along their division cycle. Both strains displayed temperature-dependent diel changes in cell size, and as a result, the relationship between temperature and average cell size varied along the day. We computed the mean cell size of new-born cells in order to test the prediction of the TSR on a single-growth stage. Our work reconciles previous inconsistent results when testing the TSR on unicellular organisms, and shows that when a single-growth stage is considered the predicted negative response to temperature is revealed.

Synergic Effects of Temperature and Irradiance on the Physiology of the Marine Synechococcus Strain WH7803.

Understanding how microorganisms adjust their metabolism to maintain their ability to cope with short-term environmental variations constitutes one of the major current challenges in microbial ecology. Here, the best physiologically characterized marine Synechococcus strain, WH7803, was exposed to modulated light/dark cycles or acclimated to continuous high-light (HL) or low-light (LL), then shifted to various stress conditions, including low (LT) or high temperature (HT), HL and ultraviolet (UV) radiations. Physiological responses were analyzed by measuring time courses of photosystem (PS) II quantum yield, PSII repair rate, pigment ratios and global changes in gene expression. Previously published membrane lipid composition were also used for correlation analyses. These data revealed that cells previously acclimated to HL are better prepared than LL-acclimated cells to sustain an additional light or UV stress, but not a LT stress. Indeed, LT seems to induce a synergic effect with the HL treatment, as previously observed with oxidative stress. While all tested shift conditions induced the downregulation of many photosynthetic genes, notably those encoding PSI, cytochrome b6/f and phycobilisomes, UV stress proved to be more deleterious for PSII than the other treatments, and full recovery of damaged PSII from UV stress seemed to involve the neo-synthesis of a fairly large number of PSII subunits and not just the reassembly of pre-existing subunits after D1 replacement. In contrast, genes involved in glycogen degradation and carotenoid biosynthesis pathways were more particularly upregulated in response to LT. Altogether, these experiments allowed us to identify responses common to all stresses and those more specific to a given stress, thus highlighting genes potentially involved in niche acclimation of a key member of marine ecosystems. Our data also revealed important specific features of the stress responses compared to model freshwater cyanobacteria.

Unveiling membrane thermoregulation strategies in marine picocyanobacteria.

The wide latitudinal distribution of marine Synechococcus cyanobacteria partly relies on the differentiation of lineages adapted to distinct thermal environments. Membranes are highly thermosensitive cell components, and the ability to modulate their fluidity can be critical for the fitness of an ecotype in a particular thermal niche. We compared the thermophysiology of Synechococcus strains representative of major temperature ecotypes in the field. We measured growth, photosynthetic capacities and membrane lipidome variations. We carried out a metagenomic analysis of stations of the Tara Oceans expedition to describe the latitudinal distribution of the lipid desaturase genes in the oceans. All strains maintained efficient photosynthetic capacities over their different temperature growth ranges. Subpolar and cold temperate strains showed enhanced capacities for lipid monodesaturation at low temperature thanks to an additional, poorly regiospecific Δ9-desaturase. By contrast, tropical and warm temperate strains displayed moderate monodesaturation capacities but high proportions of double unsaturations in response to cold, thanks to regiospecific Δ12-desaturases. The desaturase genes displayed specific distributions directly related to latitudinal variations in ocean surface temperature. This study highlights the critical importance of membrane fluidity modulation by desaturases in the adaptive strategies of Synechococcus cyanobacteria during the colonization of novel thermal niches.

Chromatic Acclimation in Cyanobacteria: A Diverse and Widespread Process for Optimizing Photosynthesis.

Chromatic acclimation (CA) encompasses a diverse set of molecular processes that involve the ability of cyanobacterial cells to sense ambient light colors and use this information to optimize photosynthetic light harvesting. The six known types of CA, which we propose naming CA1 through CA6, use a range of molecular mechanisms that likely evolved independently in distantly related lineages of the Cyanobacteria phylum. Together, these processes sense and respond to the majority of the photosynthetically relevant solar spectrum, suggesting that CA provides fitness advantages across a broad range of light color niches. The recent discoveries of several new CA types suggest that additional CA systems involving additional light colors and molecular mechanisms will be revealed in coming years. Here we provide a comprehensive overview of the currently known types of CA and summarize the molecular details that underpin CA regulation.

Interplay between differentially expressed enzymes contributes to light color acclimation in marine Synechococcus.

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.

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

The extrinsic PsbU and PsbV proteins are known to play a critical role in stabilizing the Mn4CaO5 cluster of the PSII oxygen-evolving complex (OEC). However, most isolates of the marine cyanobacterium Prochlorococcus naturally miss these proteins, even though they have kept the main OEC protein, PsbO. A structural homology model of the PSII of such a natural deletion mutant strain (P. marinus MED4) did not reveal any obvious compensation mechanism for this lack. To assess the physiological consequences of this unusual OEC, we compared oxygen evolution between Prochlorococcus strains missing psbU and psbV (PCC 9511 and SS120) and two marine strains possessing these genes (Prochlorococcus sp. MIT9313 and Synechococcus sp. WH7803). While the low light-adapted strain SS120 exhibited the lowest maximal O2 evolution rates (Pmax per divinyl-chlorophyll a, per cell or per photosystem II) of all four strains, the high light-adapted strain PCC 9511 displayed even higher PChlmax and PPSIImax at high irradiance than Synechococcus sp. WH7803. Furthermore, thermoluminescence glow curves did not show any alteration in the B-band shape or peak position that could be related to the lack of these extrinsic proteins. This suggests an efficient functional adaptation of the OEC in these natural deletion mutants, in which PsbO alone is seemingly sufficient to ensure proper oxygen evolution. Our study also showed that Prochlorococcus strains exhibit negative net O2 evolution rates at the low irradiances encountered in minimum oxygen zones, possibly explaining the very low O2 concentrations measured in these environments, where Prochlorococcus is the dominant oxyphototroph.