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The biological carbon pump is the process by which CO 2 is transformed to organic carbon via photosynthesis, exported through sinking particles, and finally sequestered in the deep ocean. While the intensity of the pump correlates with plankton community composition, the underlying ecosystem structure driving the process remains largely uncharacterized. Here we use environmental and metagenomic data gathered during the Tara Oceans expedition to improve our understanding of carbon export in the oligotrophic ocean. We show that specific plankton communities, from the surface and deep chlorophyll maximum, correlate with carbon export at 150 m and highlight unexpected taxa such as Radiolaria and alveolate parasites, as well as Synechococcus and their phages, as lineages most strongly associated with carbon export in the subtropical, nutrient-depleted, oligotrophic ocean. Additionally, we show that the relative abundance of a few bacterial and viral genes can predict a significant fraction of the variability in carbon export in these regions. Plankton communities in the top 150 m of the nutrient-depleted, oligotrophic global ocean that are most associated with carbon export include unexpected taxa, such as Radiolaria, alveolate parasites, and Synechococcus and their phages, and point towards potential functional markers predicting a significant fraction of the variability in carbon export in these regions. Oceanic plankton associated with carbon flux Using environmental and metagenomic data collected during the Tara Oceans expedition, this study examines the plankton communities that are most strongly associated with carbon export in the top 150 metres of the nutrient-depleted, oligotrophic global ocean. This work highlights some unexpected taxa as lineages strongly associated with carbon export, including Dinophyceae and Rhizaria, and alveolate parasites, in addition to Synechococcus and their phages, and suggests that the relative abundance of just a few bacterial and viral genes can predict most of the variability in carbon export in these regions.

Cyanobacteria are emerging as attractive organisms for sustainable bioproduction. We previously described Synechococcus elongatus UTEX 2973 as the fastest growing cyanobacterium known. Synechococcus 2973 exhibits high light tolerance and an increased photosynthetic rate and produces biomass at three times the rate of its close relative, the model strain Synechococcus elongatus 7942. The two strains differ at 55 genetic loci, and some of these loci must contain the genetic determinants of rapid photoautotrophic growth and improved photosynthetic rate. Using CRISPR/Cpf1, we performed a comprehensive mutational analysis of Synechococcus 2973 and identified three specific genes, atpA, ppnK, and rpaA, with SNPs that confer rapid growth. The fast-growth–associated allele of each gene was then used to replace the wild-type alleles in Synechococcus 7942. Upon incorporation, each allele successively increased the growth rate of Synechococcus 7942; remarkably, inclusion of all three alleles drastically reduced the doubling time from 6.8 to 2.3 hours. Further analysis revealed that our engineering effort doubled the photosynthetic productivity of Synechococcus 7942. We also determined that the fast-growth–associated allele of atpA yielded an ATP synthase with higher specific activity, while that of ppnK encoded a NAD⁺ kinase with significantly improved kinetics. The rpaA SNPs cause broad changes in the transcriptional profile, as this gene is the master output regulator of the circadian clock. This pioneering study has revealed the molecular basis for rapid growth, demonstrating that limited genetic changes can dramatically improve the growth rate of a microbe by as much as threefold.

Salinity and light markedly influence cyanobacterial viability. High salinity disrupts the osmotic balance, while excess light energy affects redox potential in the cells. Regulating the ratio of saturated and unsaturated alka(e)ne and fatty acids in cyanobacteria is thought to have crucial roles in coping with these stresses by regulating membrane fluidity. In Synechococcus elongatus PCC 7942 (Syn7942), alkane is produced from fatty acid metabolites using acyl-acyl carrier protein reductase (Aar) and aldehyde-deformylating oxygenase (Ado) enzymes. However, the role of alka(e)nes and their correlation with fatty acid-related compounds, especially under salinity stress, is not yet fully understood. This study explored the significance of the natural alka(e)ne biosynthesis pathway using Syn7942. The role of alka(e)ne was assessed using single and double knockout mutants of the aar and/or ado genes in this biosynthetic process. The alka(e)ne levels and membrane lipid content exhibited an inverse relationship, correlating with cell fluidity under high-salinity and high-light conditions. The absence of alka(e)ne resulted in a severe growth phenotype of Δado and Δaar/Δado under high-salinity conditions and less severe under high-light conditions. In addition, feeding with C15:0 and/or C17:0 alkanes complemented the growth phenotype with different accumulation profiles. The Δaar mutant exhibited higher resistance to high salinity than the Syn7942 WT, indicating the importance of Ado for survival at high salinity. Overall, lipid-related compounds, especially alka(e)nes, markedly contribute to cell integrity maintenance under high-salinity conditions by regulating membrane rigidity and fluidity.

Marine picocyanobacteria, comprised of the genera Synechococcus and Prochlorococcus , are the most abundant and widespread primary producers in the ocean. More than 20 genetically distinct clades of marine Synechococcus have been identified, but their physiology and biogeography are not as thoroughly characterized as those of Prochlorococcus . Using clade-specific qPCR primers, we measured the abundance of 10 Synechococcus clades at 92 locations in surface waters of the Atlantic and Pacific Oceans. We found that Synechococcus partition the ocean into four distinct regimes distinguished by temperature, macronutrients and iron availability. Clades I and IV were prevalent in colder, mesotrophic waters; clades II, III and X dominated in the warm, oligotrophic open ocean; clades CRD1 and CRD2 were restricted to sites with low iron availability; and clades XV and XVI were only found in transitional waters at the edges of the other biomes. Overall, clade II was the most ubiquitous clade investigated and was the dominant clade in the largest biome, the oligotrophic open ocean. Co-occurring clades that occupy the same regime belong to distinct evolutionary lineages within Synechococcus , indicating that multiple ecotypes have evolved independently to occupy similar niches and represent examples of parallel evolution. We speculate that parallel evolution of ecotypes may be a common feature of diverse marine microbial communities that contributes to functional redundancy and the potential for resiliency.

The production of alkanes in a marine cyanobacterium possessing the α-olefin biosynthesis pathway was achieved by introducing an exogenous alkane biosynthesis pathway. Cyanobacterial hydrocarbons are synthesized via two separate pathways: the acyl-acyl carrier protein (ACP) reductase/aldehyde-deformylating oxygenase (AAR/ADO) pathway for the alkane biosynthesis and the α-olefin synthase (OLS) pathway for the α-olefin biosynthesis. Coexistence of these pathways has not yet been reported. In this study, the marine cyanobacterium Synechococcus sp. NKBG15041c was shown to produce α-olefins similar to those of Synechococcus sp. PCC7002 via the α-olefin biosynthesis pathway. The production of heptadecane in Synechococcus sp. NKBG15041c was achieved by expressing the AAR/ADO pathway genes from Synechococcus elongatus PCC 7942. The production yields of heptadecane in Synechococcus sp. NKBG15041c varied with the expression level of the aar and ado genes. The maximal yield of heptadecane was 4.2 ± 1.2 μg/g of dried cell weight in the transformant carrying a homologous promoter. Our results also suggested that the effective activation of ADO may be more important for the enhancement of alkane production by cyanobacteria.

Cyanobacteria, a group of photosynthetic prokaryotes, are attractive hosts for biotechnological applications. It is envisaged that future biorefineries will deploy engineered cyanobacteria for the conversion of carbon dioxide to useful chemicals via light-driven, endergonic reactions. Fast-growing, genetically amenable, and stress-tolerant cyanobacteria are desirable as chassis for such applications. The recently reported strains such as Synechococcus elongatus UTEX 2973 and PCC 11801 hold promise, but additional strains may be needed for the ongoing efforts of metabolic engineering. Here, we report a novel, fast-growing, and naturally transformable cyanobacterium, S. elongatus PCC 11802, that shares 97% genome identity with its closest neighbor S. elongatus PCC 11801. The new isolate has a doubling time of 2.8 h at 1% CO 2 , 1000 µmole photons.m −2 .s −1 and grows faster under high CO 2 and temperature compared to PCC 11801 thus making it an attractive host for outdoor cultivations and eventual applications in the biorefinery. Furthermore, S. elongatus PCC 11802 shows higher levels of key intermediate metabolites suggesting that this strain might be better suited for achieving high metabolic flux in engineered pathways. Importantly, metabolite profiles suggest that the key enzymes of the Calvin cycle are not repressed under elevated CO 2 in the new isolate, unlike its closest neighbor.

Phytoplankton-bacteria interactions serve as a crucial biological network linking primary production and nutrient cycling in marine ecosystems. In the context of global change, the upper ocean inevitably faces increased warming and iron limitation, which will shift primary producer composition toward Synechococcus and impact its nutrient exchanges with co-existing bacteria. The changes in this fundamental and widespread microbial interaction may affect the stability of nutrient cycling, yet its universal response under warming and iron limitation remains poorly understood. Our research reveals contrasting responses of oligotrophic and eutrophic Synechococcus -bacteria interactions under the same stress, driven by stronger metabolic dependencies in the oligotrophic co-culture but greater individual competitiveness in the eutrophic one. These findings emphasize the importance of cooperative heterotrophic bacteria for host survival and imply a non-uniform co-evolution of in situ microbial interactions across different marine ecosystems in the future.

The factors that control elemental ratios within phytoplankton, like carbon:nitrogen:phosphorus (C:N:P), are key to biogeochemical cycles. Previous studies have identified relationships between nutrient-limited growth and elemental ratios in large eukaryotes, but little is known about these interactions in small marine phytoplankton like the globally important Cyanobacteria. To improve our understanding of these interactions in picophytoplankton, we asked how cellular elemental stoichiometry varies as a function of steady-state, N- and P-limited growth in laboratory chemostat cultures of Synechococcus WH8102. By combining empirical data and theoretical modeling, we identified a previously unrecognized factor (growth-dependent variability in cell size) that controls the relationship between nutrient-limited growth and cellular elemental stoichiometry. To predict the cellular elemental stoichiometry of phytoplankton, previous theoretical models rely on the traditional Droop model, which purports that the acquisition of a single limiting nutrient suffices to explain the relationship between a cellular nutrient quota and growth rate. Our study, however, indicates that growth-dependent changes in cell size have an important role in regulating cell nutrient quotas. This key ingredient, along with nutrient-uptake protein regulation, enables our model to predict the cellular elemental stoichiometry of Synechococcus across a range of nutrient-limited conditions. Our analysis also adds to the growth rate hypothesis , suggesting that P-rich biomolecules other than nucleic acids are important drivers of stoichiometric variability in Synechococcus . Lastly, by comparing our data with field observations, our study has important ecological relevance as it provides a framework for understanding and predicting elemental ratios in ocean regions where small phytoplankton like Synechococcus dominates.

It is important to obtain abundant sugar feedstocks economically and sustainably for bio-fermentation industry, especially for producing cheap biofuels and biochemicals. Besides plant biomass, photosynthetic cyanobacteria have also been considered to be potential microbe candidates for sustainable production of carbohydrate feedstocks. As the fastest growing cyanobacterium reported so far, Synechococcus elongatus UTEX 2973 ( Syn 2973) might have huge potential for bioproduction. In this study, we explored the potentials of this strain as photo-bioreactors for sucrose and glycogen production. Under nitrogen-replete condition, Syn 2973 could accumulate glycogen with a rate of 0.75 g L −1  day −1 at the exponential phase and reach a glycogen content as high as 51 % of the dry cell weight (DCW) at the stationary phase. By introducing a sucrose transporter CscB, Syn 2973 was endowed with an ability to secrete over 94 % sucrose out of cells under salt stress condition. The highest extracellular sucrose productivity reached 35.5 mg L −1  h −1 for the Syn 2973 strain expressing cscB , which contained the similar amounts of intracellular glycogen with the wild type. Potassium chloride was firstly proved to induce sucrose accumulation as well as sodium chloride in Syn 2973. By semi-continuous culturing, 8.7 g L −1 sucrose was produced by the cscB -expressing strain of Syn 2973 in 21 days. These results support that Syn 2973 is a promising candidate with great potential for production of sugars.