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      Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in Prochlorococcus

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          Abstract

          Previous studies showed differences in the regulatory response to C/N balance in Prochlorococcus with respect to other cyanobacteria, but no information was available about its causes, or the ecological advantages conferred to thrive in oligotrophic environments. We addressed the changes in key enzymes (glutamine synthetase, isocitrate dehydrogenase) and the ntcA gene (the global nitrogen regulator) involved in C/N metabolism and its regulation, in three model Prochlorococcus strains: MED4, SS120, and MIT9313. We observed a remarkable level of diversity in their response to azaserine, a glutamate synthase inhibitor which increases the concentration of the key metabolite 2-oxoglutarate, used to sense the C/N balance by cyanobacteria. Besides, we studied the binding between the global nitrogen regulator (NtcA) and the promoter of the glnA gene in the same Prochlorococcus strains, and its dependence on the 2-oxoglutarate concentration, by using isothermal titration calorimetry, surface plasmon resonance, and electrophoretic mobility shift. Our results show a reduction in the responsiveness of NtcA to 2-oxoglutarate in Prochlorococcus, especially in the MED4 and SS120 strains. This suggests a trend to streamline the regulation of C/N metabolism in late-branching Prochlorococcus strains (MED4 and SS120), in adaptation to the rather stable conditions found in the oligotrophic ocean gyres where this microorganism is most abundant.

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          Most cited references 61

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          Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus.

          The Cyanobacteria Prochlorococcus and Synechococcus account for a substantial fraction of marine primary production. Here, we present quantitative niche models for these lineages that assess present and future global abundances and distributions. These niche models are the result of neural network, nonparametric, and parametric analyses, and they rely on >35,000 discrete observations from all major ocean regions. The models assess cell abundance based on temperature and photosynthetically active radiation, but the individual responses to these environmental variables differ for each lineage. The models estimate global biogeographic patterns and seasonal variability of cell abundance, with maxima in the warm oligotrophic gyres of the Indian and the western Pacific Oceans and minima at higher latitudes. The annual mean global abundances of Prochlorococcus and Synechococcus are 2.9 ± 0.1 × 10(27) and 7.0 ± 0.3 × 10(26) cells, respectively. Using projections of sea surface temperature as a result of increased concentration of greenhouse gases at the end of the 21st century, our niche models projected increases in cell numbers of 29% and 14% for Prochlorococcus and Synechococcus, respectively. The changes are geographically uneven but include an increase in area. Thus, our global niche models suggest that oceanic microbial communities will experience complex changes as a result of projected future climate conditions. Because of the high abundances and contributions to primary production of Prochlorococcus and Synechococcus, these changes may have large impacts on ocean ecosystems and biogeochemical cycles.
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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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              A novel free-living prochlorophyte abundant in the oceanic euphotic zone

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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                09 January 2018
                2017
                : 8
                Affiliations
                1Departamento de Bioquímica y Biología Molecular, Campus de Excelencia Internacional Agroalimentario CeiA3, Universidad de Córdoba , Córdoba, Spain
                2Institute of Biocomputation and Physics of Complex Systems (BIFI), Joint Units BIFI-IQFR-CSIC and GBsC-BIFI-CSIC, Universidad de Zaragoza , Zaragoza, Spain
                3Aragon Institute for Health Research (IIS Aragon) , Zaragoza, Spain
                4Instituto Aragonés de Ciencias de la Salud , Zaragoza, Spain
                5Centro de Investigación Biomédica en Red en el Área Temática de Enfermedades Hepáticas y Digestivas , Barcelona, Spain
                6Fundación ARAID, Gobierno de Aragón , Zaragoza, Spain
                7Professur für Mikrobiologie, Department Biologie, Friedrich-Alexander-Universität Erlangen-Nürnberg , Erlangen, Germany
                Author notes

                Edited by: George S. Bullerjahn, Bowling Green State University, United States

                Reviewed by: Lisa Moore, University of Southern Maine, United States; Branko Rihtman, University of Warwick, United Kingdom

                *Correspondence: José M. García-Fernández jmgarcia@ 123456uco.es

                This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.02641
                5767323
                Copyright © 2018 Domínguez-Martín, López-Lozano, Clavería-Gimeno, Velázquez-Campoy, Seidel, Burkovski, Díez and García-Fernández.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 7, Tables: 2, Equations: 1, References: 70, Pages: 16, Words: 11528
                Funding
                Funded by: Ministerio de Economía y Competitividad 10.13039/501100003329
                Award ID: BFU2013-44767-P
                Award ID: BFU2013-47064-P
                Award ID: BFU2016-76227-P
                Award ID: BFU2016-78232-P
                Funded by: Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía 10.13039/501100002878
                Award ID: P12-BIO-2141
                Categories
                Microbiology
                Original Research

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