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      Picocyanobacteria containing a novel pigment gene cluster dominate the brackish water Baltic Sea

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          Abstract

          Photoautotrophic picocyanobacteria harvest light via phycobilisomes (PBS) consisting of the pigments phycocyanin (PC) and phycoerythrin (PE), encoded by genes in conserved gene clusters. The presence and arrangement of these gene clusters give picocyanobacteria characteristic light absorption properties and allow the colonization of specific ecological niches. To date, a full understanding of the evolution and distribution of the PBS gene cluster in picocyanobacteria has been hampered by the scarcity of genome sequences from fresh- and brackish water-adapted strains. To remediate this, we analysed genomes assembled from metagenomic samples collected along a natural salinity gradient, and over the course of a growth season, in the Baltic Sea. We found that while PBS gene clusters in picocyanobacteria sampled in marine habitats were highly similar to known references, brackish-adapted genotypes harboured a novel type not seen in previously sequenced genomes. Phylogenetic analyses showed that the novel gene cluster belonged to a clade of uncultivated picocyanobacteria that dominate the brackish Baltic Sea throughout the summer season, but are uncommon in other examined aquatic ecosystems. Further, our data suggest that the PE genes were lost in the ancestor of PC-containing coastal picocyanobacteria and that multiple horizontal gene transfer events have re-introduced PE genes into brackish-adapted strains, including the novel clade discovered here.

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          Most cited references28

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          Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing.

          The cyanobacterial phylum encompasses oxygenic photosynthetic prokaryotes of a great breadth of morphologies and ecologies; they play key roles in global carbon and nitrogen cycles. The chloroplasts of all photosynthetic eukaryotes can trace their ancestry to cyanobacteria. Cyanobacteria also attract considerable interest as platforms for "green" biotechnology and biofuels. To explore the molecular basis of their different phenotypes and biochemical capabilities, we sequenced the genomes of 54 phylogenetically and phenotypically diverse cyanobacterial strains. Comparison of cyanobacterial genomes reveals the molecular basis for many aspects of cyanobacterial ecophysiological diversity, as well as the convergence of complex morphologies without the acquisition of novel proteins. This phylum-wide study highlights the benefits of diversity-driven genome sequencing, identifying more than 21,000 cyanobacterial proteins with no detectable similarity to known proteins, and foregrounds the diversity of light-harvesting proteins and gene clusters for secondary metabolite biosynthesis. Additionally, our results provide insight into the distribution of genes of cyanobacterial origin in eukaryotic nuclear genomes. Moreover, this study doubles both the amount and the phylogenetic diversity of cyanobacterial genome sequence data. Given the exponentially growing number of sequenced genomes, this diversity-driven study demonstrates the perspective gained by comparing disparate yet related genomes in a phylum-wide context and the insights that are gained from it.
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            Ecological genomics of marine picocyanobacteria.

            Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus numerically dominate the picophytoplankton of the world ocean, making a key contribution to global primary production. Prochlorococcus was isolated around 20 years ago and is probably the most abundant photosynthetic organism on Earth. The genus comprises specific ecotypes which are phylogenetically distinct and differ markedly in their photophysiology, allowing growth over a broad range of light and nutrient conditions within the 45 degrees N to 40 degrees S latitudinal belt that they occupy. Synechococcus and Prochlorococcus are closely related, together forming a discrete picophytoplankton clade, but are distinguishable by their possession of dissimilar light-harvesting apparatuses and differences in cell size and elemental composition. Synechococcus strains have a ubiquitous oceanic distribution compared to that of Prochlorococcus strains and are characterized by phylogenetically discrete lineages with a wide range of pigmentation. In this review, we put our current knowledge of marine picocyanobacterial genomics into an environmental context and present previously unpublished genomic information arising from extensive genomic comparisons in order to provide insights into the adaptations of these marine microbes to their environment and how they are reflected at the genomic level.
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              Ray Meta: scalable de novo metagenome assembly and profiling

              Voluminous parallel sequencing datasets, especially metagenomic experiments, require distributed computing for de novo assembly and taxonomic profiling. Ray Meta is a massively distributed metagenome assembler that is coupled with Ray Communities, which profiles microbiomes based on uniquely-colored k-mers. It can accurately assemble and profile a three billion read metagenomic experiment representing 1,000 bacterial genomes of uneven proportions in 15 hours with 1,024 processor cores, using only 1.5 GB per core. The software will facilitate the processing of large and complex datasets, and will help in generating biological insights for specific environments. Ray Meta is open source and available at http://denovoassembler.sf.net.
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                Author and article information

                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group
                1751-7362
                1751-7370
                September 2014
                13 March 2014
                1 September 2014
                : 8
                : 9
                : 1892-1903
                Affiliations
                [1 ]Department of Ecology, Environment and Plant Sciences, Stockholm University, Science for Life Laboratory , Solna, Sweden
                [2 ]Microbial and Environmental Genomics, J Craig Venter Institute , San Diego, CA, USA
                [3 ]Informatics Group, J Craig Venter Institute , San Diego, CA, USA
                Author notes
                [* ]Department of Ecology, Environment and Plant Sciences, Stockholm University, Science for Life Laboratory , Tomtebodavà gen 23B, Solna SE-17165, Sweden. E-mail: john.larsson@ 123456su.se
                Article
                ismej201435
                10.1038/ismej.2014.35
                4139726
                24621524
                38e803cf-93a5-4446-83fe-9bb5d12b6234
                Copyright © 2014 International Society for Microbial Ecology

                This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/

                History
                : 04 December 2013
                : 27 January 2014
                : 28 January 2014
                Categories
                Original Article

                Microbiology & Virology
                cyanobacteria,phycobilisome,pigment,horizontal gene transfer,baltic sea,ecology

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