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      Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage

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          Abstract

          Background

          Bathycoccus prasinos is an extremely small cosmopolitan marine green alga whose cells are covered with intricate spider's web patterned scales that develop within the Golgi cisternae before their transport to the cell surface. The objective of this work is to sequence and analyze its genome, and to present a comparative analysis with other known genomes of the green lineage.

          Research

          Its small genome of 15 Mb consists of 19 chromosomes and lacks transposons. Although 70% of all B. prasinos genes share similarities with other Viridiplantae genes, up to 428 genes were probably acquired by horizontal gene transfer, mainly from other eukaryotes. Two chromosomes, one big and one small, are atypical, an unusual synapomorphic feature within the Mamiellales. Genes on these atypical outlier chromosomes show lower GC content and a significant fraction of putative horizontal gene transfer genes. Whereas the small outlier chromosome lacks colinearity with other Mamiellales and contains many unknown genes without homologs in other species, the big outlier shows a higher intron content, increased expression levels and a unique clustering pattern of housekeeping functionalities. Four gene families are highly expanded in B. prasinos, including sialyltransferases, sialidases, ankyrin repeats and zinc ion-binding genes, and we hypothesize that these genes are associated with the process of scale biogenesis.

          Conclusion

          The minimal genomes of the Mamiellophyceae provide a baseline for evolutionary and functional analyses of metabolic processes in green plants.

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          Most cited references51

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          Horizontal gene transfer in eukaryotic evolution.

          Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.
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            Global phytoplankton decline over the past century.

            In the oceans, ubiquitous microscopic phototrophs (phytoplankton) account for approximately half the production of organic matter on Earth. Analyses of satellite-derived phytoplankton concentration (available since 1979) have suggested decadal-scale fluctuations linked to climate forcing, but the length of this record is insufficient to resolve longer-term trends. Here we combine available ocean transparency measurements and in situ chlorophyll observations to estimate the time dependence of phytoplankton biomass at local, regional and global scales since 1899. We observe declines in eight out of ten ocean regions, and estimate a global rate of decline of approximately 1% of the global median per year. Our analyses further reveal interannual to decadal phytoplankton fluctuations superimposed on long-term trends. These fluctuations are strongly correlated with basin-scale climate indices, whereas long-term declining trends are related to increasing sea surface temperatures. We conclude that global phytoplankton concentration has declined over the past century; this decline will need to be considered in future studies of marine ecosystems, geochemical cycling, ocean circulation and fisheries.
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              Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features.

              The green lineage is reportedly 1,500 million years old, evolving shortly after the endosymbiosis event that gave rise to early photosynthetic eukaryotes. In this study, we unveil the complete genome sequence of an ancient member of this lineage, the unicellular green alga Ostreococcus tauri (Prasinophyceae). This cosmopolitan marine primary producer is the world's smallest free-living eukaryote known to date. Features likely reflecting optimization of environmentally relevant pathways, including resource acquisition, unusual photosynthesis apparatus, and genes potentially involved in C(4) photosynthesis, were observed, as was downsizing of many gene families. Overall, the 12.56-Mb nuclear genome has an extremely high gene density, in part because of extensive reduction of intergenic regions and other forms of compaction such as gene fusion. However, the genome is structurally complex. It exhibits previously unobserved levels of heterogeneity for a eukaryote. Two chromosomes differ structurally from the other eighteen. Both have a significantly biased G+C content, and, remarkably, they contain the majority of transposable elements. Many chromosome 2 genes also have unique codon usage and splicing, but phylogenetic analysis and composition do not support alien gene origin. In contrast, most chromosome 19 genes show no similarity to green lineage genes and a large number of them are specialized in cell surface processes. Taken together, the complete genome sequence, unusual features, and downsized gene families, make O. tauri an ideal model system for research on eukaryotic genome evolution, including chromosome specialization and green lineage ancestry.
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                Author and article information

                Journal
                Genome Biol
                Genome Biol
                Genome Biology
                BioMed Central
                1465-6906
                1465-6914
                2012
                24 August 2012
                : 13
                : 8
                : R74
                Affiliations
                [1 ]CNRS, UMR 7232, Observatoire Océanologique, Banyuls-sur-Mer, France
                [2 ]UPMC Univ Paris 06, UMR 7232, Observatoire Océanologique, Banyuls-sur-Mer, France
                [3 ]Department of Plant Systems Biology, VIB, Technologiepark 927, B-9052 Ghent, Belgium
                [4 ]Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium
                [5 ]Genoscope, CEA, Institut de Génomique, 2 rue Gaston Crémieux CP5706, 91057 Evry cedex, France
                [6 ]Department of Biotechnology, Norwegian University of Science and Technology (NTNU), 7491 Trondheim, Norway †These two authors contributed equally to this work
                Article
                gb-2012-13-8-r74
                10.1186/gb-2012-13-8-r74
                3491373
                22925495
                f06da889-17a9-4957-979e-1d828690cc7c
                Copyright ©2012 Moreau et al.; licensee BioMed Central Ltd.

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 April 2012
                : 15 August 2012
                : 24 August 2012
                Categories
                Research

                Genetics
                Genetics

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