Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in Prochlorococcus
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 enzy...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2017.02641/full |
| _version_ | 1818058202038665216 |
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| author | María A. Domínguez-Martín Antonio López-Lozano Rafael Clavería-Gimeno Rafael Clavería-Gimeno Rafael Clavería-Gimeno Adrián Velázquez-Campoy Adrián Velázquez-Campoy Adrián Velázquez-Campoy Adrián Velázquez-Campoy Gerald Seidel Andreas Burkovski Jesús Díez José M. García-Fernández |
| author_facet | María A. Domínguez-Martín Antonio López-Lozano Rafael Clavería-Gimeno Rafael Clavería-Gimeno Rafael Clavería-Gimeno Adrián Velázquez-Campoy Adrián Velázquez-Campoy Adrián Velázquez-Campoy Adrián Velázquez-Campoy Gerald Seidel Andreas Burkovski Jesús Díez José M. García-Fernández |
| author_sort | María A. Domínguez-Martín |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-10T12:56:52Z |
| format | Article |
| id | doaj.art-cf05eb6bd36e403183e6bd3a3d039a79 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-10T12:56:52Z |
| publishDate | 2018-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-cf05eb6bd36e403183e6bd3a3d039a792022-12-22T01:48:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-01-01810.3389/fmicb.2017.02641298355Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in ProchlorococcusMaría A. Domínguez-Martín0Antonio López-Lozano1Rafael Clavería-Gimeno2Rafael Clavería-Gimeno3Rafael Clavería-Gimeno4Adrián Velázquez-Campoy5Adrián Velázquez-Campoy6Adrián Velázquez-Campoy7Adrián Velázquez-Campoy8Gerald Seidel9Andreas Burkovski10Jesús Díez11José M. García-Fernández12Departamento de Bioquímica y Biología Molecular, Campus de Excelencia Internacional Agroalimentario CeiA3, Universidad de Córdoba, Córdoba, SpainDepartamento de Bioquímica y Biología Molecular, Campus de Excelencia Internacional Agroalimentario CeiA3, Universidad de Córdoba, Córdoba, SpainInstitute of Biocomputation and Physics of Complex Systems (BIFI), Joint Units BIFI-IQFR-CSIC and GBsC-BIFI-CSIC, Universidad de Zaragoza, Zaragoza, SpainAragon Institute for Health Research (IIS Aragon), Zaragoza, SpainInstituto Aragonés de Ciencias de la Salud, Zaragoza, SpainInstitute of Biocomputation and Physics of Complex Systems (BIFI), Joint Units BIFI-IQFR-CSIC and GBsC-BIFI-CSIC, Universidad de Zaragoza, Zaragoza, SpainAragon Institute for Health Research (IIS Aragon), Zaragoza, SpainCentro de Investigación Biomédica en Red en el Área Temática de Enfermedades Hepáticas y Digestivas, Barcelona, SpainFundación ARAID, Gobierno de Aragón, Zaragoza, SpainProfessur für Mikrobiologie, Department Biologie, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, GermanyProfessur für Mikrobiologie, Department Biologie, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, GermanyDepartamento de Bioquímica y Biología Molecular, Campus de Excelencia Internacional Agroalimentario CeiA3, Universidad de Córdoba, Córdoba, SpainDepartamento de Bioquímica y Biología Molecular, Campus de Excelencia Internacional Agroalimentario CeiA3, Universidad de Córdoba, Córdoba, SpainPrevious 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.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02641/fullProchlorococcuscyanobacteria2-oxoglutaratestreamlined regulationC/N balance |
| spellingShingle | María A. Domínguez-Martín Antonio López-Lozano Rafael Clavería-Gimeno Rafael Clavería-Gimeno Rafael Clavería-Gimeno Adrián Velázquez-Campoy Adrián Velázquez-Campoy Adrián Velázquez-Campoy Adrián Velázquez-Campoy Gerald Seidel Andreas Burkovski Jesús Díez José M. García-Fernández Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in Prochlorococcus Frontiers in Microbiology Prochlorococcus cyanobacteria 2-oxoglutarate streamlined regulation C/N balance |
| title | Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in Prochlorococcus |
| title_full | Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in Prochlorococcus |
| title_fullStr | Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in Prochlorococcus |
| title_full_unstemmed | Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in Prochlorococcus |
| title_short | Differential NtcA Responsiveness to 2-Oxoglutarate Underlies the Diversity of C/N Balance Regulation in Prochlorococcus |
| title_sort | differential ntca responsiveness to 2 oxoglutarate underlies the diversity of c n balance regulation in prochlorococcus |
| topic | Prochlorococcus cyanobacteria 2-oxoglutarate streamlined regulation C/N balance |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2017.02641/full |
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