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      Differential expression of the glucose transporter gene glcH in response to glucose and light in marine picocyanobacteria

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          Abstract

          Background

          Our team discovered that Prochlorococcus can take up glucose, in a process that changes the transcriptional pattern of several genes involved in glucose metabolization. We have also shown that glcH encodes a very high affinity glucose transporter, and that glucose is taken up by natural Prochlorococcus populations. We demonstrated that the kinetic parameters of glucose uptake show significant diversity in different Prochlorococcus and Synechococcus strains. Here, we tested whether the transcriptional response of glcH to several glucose concentrations and light conditions was also different depending on the studied strain.

          Methods

          Cultures were grown in the light, supplemented with five different glucose concentrations or subjected to darkness, and cells harvested after 24 h of treatment. qRT-PCR was used to determine glcH expression in four Prochlorococcus and two Synechococcus strains.

          Results

          In all studied strains glcH was expressed in the absence of glucose, and it increased upon glucose addition to cultures. The changes differed depending on the strain, both in the magnitude and in the way cells responded to the tested glucose concentrations. Unlike the other strains, Synechococcus BL107 showed the maximum glucose uptake at 5 nM glucose. Darkness induced a strong decrease in glcH expression, especially remarkable in Prochlorococcus MIT9313.

          Discussion

          Our results suggest that marine picocyanobacteria are actively monitoring the availability of glucose, to upregulate glcH expression in order to exploit the presence of sugars in the environment. The diverse responses observed in different strains suggest that the transcriptional regulation of glucose uptake has been adjusted by evolutive selection. Darkness promotes a strong decrease in glcH expression in all studied strains, which fits with previous results on glucose uptake in Prochlorococcus. Overall, this work reinforces the importance of mixotrophy for marine picocyanobacteria.

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          Most cited references55

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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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              The genome of a motile marine Synechococcus.

              Marine unicellular cyanobacteria are responsible for an estimated 20-40% of chlorophyll biomass and carbon fixation in the oceans. Here we have sequenced and analysed the 2.4-megabase genome of Synechococcus sp. strain WH8102, revealing some of the ways that these organisms have adapted to their largely oligotrophic environment. WH8102 uses organic nitrogen and phosphorus sources and more sodium-dependent transporters than a model freshwater cyanobacterium. Furthermore, it seems to have adopted strategies for conserving limited iron stores by using nickel and cobalt in some enzymes, has reduced its regulatory machinery (consistent with the fact that the open ocean constitutes a far more constant and buffered environment than fresh water), and has evolved a unique type of swimming motility. The genome of WH8102 seems to have been greatly influenced by horizontal gene transfer, partially through phages. The genetic material contributed by horizontal gene transfer includes genes involved in the modification of the cell surface and in swimming motility. On the basis of its genome, WH8102 is more of a generalist than two related marine cyanobacteria.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ Inc. (San Diego, USA )
                2167-8359
                11 January 2019
                2019
                : 6
                : e6248
                Affiliations
                Departamento de Bioquímica y Biología Molecular, Campus de Excelencia Internacional Agroalimentario CeiA3, Universidad de Córdoba , Córdoba, Spain
                Author information
                http://orcid.org/0000-0002-1346-3528
                http://orcid.org/0000-0003-2983-1214
                Article
                6248
                10.7717/peerj.6248
                6330958
                30648008
                cf78173d-21f0-4205-9d88-4fed98c71690
                © 2019 Moreno-Cabezuelo et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 24 October 2018
                : 9 December 2018
                Funding
                Funded by: Proyectos de Excelencia, Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía, Spain
                Award ID: P12-BIO-2141
                Funded by: Ministerio de Economía y Competitividad, Government of Spain
                Award ID: BFU-2016-76227-P
                Funded by: European Social Fund from the European Union, and Universidad de Córdoba (Programa Propio de Investigación
                José Ángel Moreno Cabezuelo and Antonio López-Lozano received a doctoral and post-doctoral grant, respectively, from project P12-BIO-2141 (Proyectos de Excelencia, Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía, Spain). This work was supported by grants P12-BIO-2141 (Proyectos de Excelencia, Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía, Spain), BFU-2016-76227-P (Ministerio de Economía y Competitividad, Government of Spain), cofunded by the European Social Fund from the European Union, and Universidad de Córdoba (Programa Propio de Investigación). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Ecology
                Marine Biology
                Microbiology
                Molecular Biology
                Biological Oceanography

                glucose uptake,gene expression,transcriptional regulation,marine picocyanobacteria,darkness

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