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Glucose Uptake in Marine Cyanobacteria: Regulation, Expression of The Glucose uptake in marine cyanobacteria: regulation, expression of the transporter and effects on the proteome and metabolome José Ángel Moreno Cabezuelo PhD Thesis Supervisors: Jesús Díez Dapena José Manuel García-Fernández PhD in Biological Sciences PhD in Biological Sciences Professor of the Dpt. of Biochemistry Professor of the Dpt. of Biochemistry and Molecular Biology and Molecular Biology Universidad de Córdoba TITULO: Glucose uptake in marine cyanobacteria: regulation, expression of the transporter and effects on the proteome and metabolome AUTOR: José Ángel Moreno Cabezuelo © Edita: UCOPress. 2019 Campus de Rabanales Ctra. Nacional IV, Km. 396 A 14071 Córdoba https://www.uco.es/ucopress/index.php/es/ [email protected] TÍTULO DE LA TESIS: Glucose uptake in marine cyanobacteria: regulation, expression of the transporter and effects on the proteome and metabolome DOCTORANDO: José Ángel Moreno Cabezuelo INFORME RAZONADO DEL/DE LOS DIRECTOR/ES DE LA TESIS (se hará mención a la evolución y desarrollo de la tesis, así como a trabajos y publicaciones derivados de la misma). El trabajo realizado por el doctorando José Ángel Moreno Cabezuelo se puede considerar de excelente. Durante el tiempo transcurrido desde su inicio (tres años y tres meses), ha realizado un estudio exhaustivo sobre los efectos de la adición de glucosa en la expresión del gen glcH, codificante de un transportador de glucosa de alta afinidad en cianobacterias marinas. Además, ha usado técnicas de proteómica y metabolómica de última generación para analizar el efecto de la glucosa sobre el metabolismo de tres estirpes de Prochlorococcus y tres de Synechococcus. Es de reseñar que este es uno de los primeros estudios en el que se han utilizado ambas técnicas en picocianobacterias marinas. Por otra parte, ha construido estirpes mutantes en dos residuos aminoacídicos esenciales del transportador GlcH. Y por último, ha conseguido sobreexpresar y purificar dicho transportador, con el objetivo de realizar estudios estructurales sobre el mismo en el futuro. La formación de José Ángel Moreno Cabezuelo ha sido de muy alta calidad, en nuestra opinión, aprendiendo tanto técnicas de bioquímica (expresión y purificación de proteínas, proteómica) como de biología molecular (estudios de expresión génica, diseño y construcción de mutantes), lo que le permitirá abordar nuevos retos científicos en el futuro con gran capacidad. Además, ha realizado un considerable esfuerzo de lectura e integración de bibliografía para la escritura de su tesis doctoral, que se ha reflejado en un manuscrito de alta calidad, escrito íntegramente en inglés. Es de reseñar que su tesis opta a la mención internacional, al haber realizado una estancia de tres meses en el laboratorio de la Dra. Margarida Archer (Oeiras, Portugal), en el que aprendió las técnicas de optimización de expresión de proteínas de membrana, como el transportador sujeto de la tesis. Durante el desarrollo de estos estudios, José Ángel Moreno Cabezuelo ha realizado diversas comunicaciones en forma de póster y charla en congresos nacionales e internacionales, y además ha publicado un primer artículo en la revista PeerJ, en el que se describen los resultados obtenidos sobre expresión génica: Moreno-Cabezuelo JA, López-Lozano A, Díez J & García-Fernández JM (2019) Differential glcH expression in response to glucose and light in marine picocyanobacteria. PeerJ 6:e6248. doi 10.7717/peerj.6248. Además, hay en preparación un segundo artículo, en el que se integrarán los resultados de proteómica y metabolómica. Los resultados obtenidos con los mutantes en residuos aminoacídicos esenciales de GlcH se presentarán en un manuscrito adicional. Consideramos que el doctorando José Ángel Moreno Cabezuelo ha realizado una labor extraordinaria para obtener su tesis doctoral. Por todo ello, se autoriza la presentación de la tesis doctoral. Córdoba, 22 de abril de 2019 Firma de los directores Jesús Díez Dapena José Manuel García Fernández ABSTRACT Prochlorococcus and Synechococcus are the two photosynthetic organisms more abundant on Earth. Both have become a model in marine ecology and are responsible for a significant part of the global primary production. Previous results from our team demonstrated that Prochlorococcus can take up glucose, finding an increase in genes involved in its metabolization upon glucose addition. Later it was shown that the Pro1404/glcH gene encodes a biphasic glucose transporter in Prochlorococcus sp. strain SS120. Also, glucose uptake was detected in natural Prochlorococcus populations in the Atlantic Ocean. Given that this gene is present in all Prochlorococcus and Synechococcus strains, we decided to perform comparative experiments to assess the capabilities for glucose utilization in several representative strains from both genera, subjected to different glucose concentrations and also to darkness. To this goal, we used a double approach, proteomics and metabolomics, analyzing also the effect of darkness on the protein expression when glucose is available. Our working hypothesis is that mixotrophy confers an evolutive advantage to Prochlorococcus over other microorganisms which share the ecological niche (oligotrophic areas in the oceans). The observed changes in glcH expression after addition of increasing concentrations of glucose indicate that Prochlorococcus and Synechococcus detect those concentrations, adapting the transporter expression accordingly. The decrease of glcH expression induced by darkness shows the active nature of glucose uptake in marine picocyanobacteria. This decrease is stronger in Prochlorococcus sp. strain MIT9313. The metabolomic and proteomic results show that Prochlorococcus and Synechococcus take up and use glucose. The addition of 5 mM glucose led to a strong metabolic change towards general anabolic patterns in all studied strains. Finally, the high affinity glucose transporter GlcH from Prochlorococcus sp. strain SS120 has been overexpressed and purified, with the goal of performing structural studies in the future. Besides, two mutants in essential amino acid residues of the glucose transporter GlcH from Prochlorococcus sp. strain SS120 have been constructed. Resumen Procholorococcus y Synechococcus son los dos organismos fotosintéticos más abundantes en la Tierra. Ambos se han convertido en modelo en ecología marina, y son responsables de una parte importante de la producción primaria global. Resultados previos en nuestro grupo demostraron que Prochlorococcus puede transportar glucosa, observando un aumento en la expresión de genes implicados en su metabolización tras la adición de glucosa. Posteriormente, se demostró que el gen Pro1404/glcH codifica un transportador de glucosa de cinética bifásica en Prochlorococcus sp. SS120. Además, se detectó transporte de glucosa en poblaciones naturales de Prochlorococcus en el Atlántico. Dado que este gen está presente en todas las estirpes de Prochlorococcus y Synechococcus, decidimos realizar experimentos comparativos que abordaran las capacidades de utilización de glucosa en varias estirpes representativas de ambos géneros, sometidas a diferentes concentraciones de glucosa y también a la oscuridad. Para ello utilizamos una doble aproximación proteómica y metabolómica, analizando además el efecto de la oscuridad sobre la expresión de proteínas cuando hay glucosa disponible. Nuestra hipótesis de trabajo es que la mixotrofía confiere una ventaja evolutiva a Procholorococcus frente a otros microorganismos con los que comparte el nicho ecológico (zonas oligotróficas de los océanos). Los cambios observados en la expresión de glcH después de la adición de concentraciones crecientes de glucosa indican que Prochlorococcus y Synechococcus detectan estas concentraciones, adaptando la expresión del transportador en consecuencia. La disminución de la expresión de glcH inducida por la oscuridad muestra la naturaleza activa de la captación de glucosa en las picocianobacterias marinas. Esta disminución es más pronunciada en Prochlorococcus sp. MIT9313. Los resultados de metabolómica y proteómica demuestran que Prochlorococcus y Synechococcus absorben y utilizan glucosa. La adición de 5 mM de glucosa condujo a un fuerte cambio metabólico hacia patrones anabólicos generales en todas las estirpes estudiadas. Finalmente, el transportador de glucosa de alta afinidad GlcH de Prochlorococcus sp. SS120 ha sido sobreexpresado y purificado, con el fin de realizar estudios estructurales posteriormente. Además, se han construido por mutagénesis dirigida dos mutantes en residuos de aminoácidos esenciales del transportador de glucosa GlcH de Prochlorococcus sp. SS120. “El mejor maestro en la vida es la experiencia. Te cobra caro, pero explica bien” Anónimo “Lo que hacemos en la vida tiene su eco en la eternidad” Gladiator A mis padres A mi hermano Agradezco profundamente a todas las personas que me han ayudado apoyado y acompañado durante este “camino” llamado tesis doctoral En primer lugar, a mis directores José Manuel y Jesús por acogerme en su grupo, tratarme de la mejor manera, ser grandiosos compañeros de trabajo y antes que jefes, excelentes amigos y tener una calidad humana inmensurable, gracias por confiar en mí y darme la oportunidad de ser doctor, y poder llevar a cabo una carrera investigadora, siempre os estaré eternamente agradecidos. La realización de la presente tesis es fruto de las orientaciones, sugerencias y estímulos de mis tutores, los cuales me han conducido durante estos años con talante abierto y generoso, guiándome y mostrando en cada momento
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