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2009Santos Beneit, Fernando Universidad de León Departamento de Biología Molecular Mecanismo molecular del control por fosfato de la cascada de expresión de los genes de biosíntesis de metabolitos secundarios en Streptomyces coelicolor Fernando Santos Beneit León, 2009 Memoria presentada por Fernando Santos Beneit para optar al grado de Doctor en Biología Universidad de León INFORME DEL DIRECTOR DE LA TESIS (Art. 11.3 del R.D. 56/2005) Los Dres. D. Juan Francisco Martín Martín y D. Antonio Rodríguez García como directores1 de la Tesis Doctoral titulada “Mecanismo molecular del control por fosfato de la cascada de expresión de los genes de biosíntesis de metabolitos secundarios en Streptomyces coelicolor” realizada por D. Fernando Santos Beneit en el Departamento de Biología Molecular, informan favorablemente el depósito de la misma, dado que reúne las condiciones necesarias para su defensa. Lo que firmo, para dar cumplimiento al art. 11.3 del R.D. 56/2005, en León a de Diciembre de 2009. 1 Si la Tesis está dirigida por más de un Director tienen que constar los datos de cada uno y han de firmar todos ellos. Universidad de León ADMISIÓN A TRÁMITE DEL DEPARTAMENTO (Art. 11.3 del R.D. 56/2005 y Norma 7ª de las Complementarias de la ULE) El Departamento de Biología Molecular en su reunión celebrada el día * de * de 2009 ha acordado dar su conformidad a la admisión a trámite de lectura de la Tesis Doctoral titulada “Mecanismo molecular del control por fosfato de la cascada de expresión de los genes de biosíntesis de metabolitos secundarios en Streptomyces coelicolor” dirigida por el Dr. D. Juan Francisco Martín Martín y el Dr. D. Antonio Rodríguez García, elaborada por D. Fernando Santos Beneit. Lo que firmo, para dar cumplimiento al art. 11.3 del R.D. 56/2005, en León a de Diciembre de 2009. El Secretario, Fdo.: D. Jesús Manuel Aparicio Fernández Vº Bº El Director del Departamento, Fdo.: D. Pedro Calvo Fernández A mi familia “No estudio por saber más, sino por ignorar menos” SOR JUANA INÉS DE LA CRUZ (1651 – 1695) Indice 1. Introducción ........................................................................... 19 1.1. Streptomyces coelicolor: organismo modelo del género Streptomyces ............................................................................................. 19 1.1.1. Características generales del género Streptomyces y reseña histórica del grupo de los actinomicetos......................................................................... 19 1.1.2. Genética de Streptomyces ..................................................................................... 21 1.1.3. Ciclo de vida de Streptomyces ............................................................................... 23 1.1.4. Streptomyces en la medicina, agricultura, ecología e industria farmacológica .................................................................................................................. 25 1.1.5. Control por fosfato de la biosíntesis de metabolitos secundarios en especies del género Streptomyces .................................................................................. 28 1.1.6. La regulación de la biosíntesis de antibióticos incluye reguladores específicos y globales ...................................................................................................... 30 1.1.7. Regulación coordinada de la diferenciación morfológica y la producción de antibióticos en Streptomyces .................................................................. 32 1.1.8. Señales intercelulares en Streptomyces: γ‐butirolactonas ................................... 34 1.1.9. Un proceso de muerte celular precede a la producción de antibióticos en Streptomyces .......................................................................................... 35 1.1.10. Streptomyces coelicolor: características generales ............................................. 36 1.2. El regulón pho ..................................................................................... 40 1.2.1. Transporte de compuestos que contienen fósforo en las bacterias ..................... 41 1.2.2. El regulón pho está controlado por un sistema de dos componentes ................. 44 1.2.3. Interacción de los sistemas PhoR‐PhoB y PhoR‐PhoP de E. coli y B. subtilis con otros sistemas ........................................................................................... 45 1.2.4. Implicación del regulón pho en la respuesta al estrés y la patogenicidad microbiana ............................................................................................... 47 1.2.5. Activación y desactivación del regulón pho: modelo de Wanner ......................... 48 1.2.6. Captación de la señal de escasez de fosfato: PhoR, PhoU y PstS .......................... 50 1.2.7. Efecto de la fosforilación en la activación y unión de PhoB/PhoP al DNA .................................................................................................................................. 52 1.2.8. Unión de PhoB al DNA: cajas PHO ......................................................................... 56 1.2.9. Regulación transcripcional ejercida por PhoB/PhoP: interacción con la RNA polimerasa ........................................................................................................... 58 Bibliografía ....................................................................................................................... 61 2. Publicaciones ......................................................................... 91 2.1. Genome‐wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant ................................................... 93 2.2. Phosphate‐dependent regulation of the low and high affinity transport systems in the soil actinomycete Streptomyces coelicolor ........................................................................... 113 2.3. Crosstalk between two global regulators in Streptomyces: PhoP and AfsR interact in the control of afsS, pstS and phoRP transcription ............................................................................................ 129 2.4. Phosphate control over nitrogen metabolism in Streptomyces coelicolor: direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP ......................................................................................... 145 2.5. Phosphate and carbon source regulation of two PhoP‐ dependent glycerophosphodiester phosphodiesterase genes of Streptomyces coelicolor ...................................................................... 159 3. Discusión .............................................................................. 173 3.1. Aportación de la estructura operadora de pitH2, glpQ1, glpQ2 y afsS al conocimiento de la caja PHO en Streptomyces coelicolor .................................................................................................. 173 3.2. Inducción y represión génica por la proteína PhoP ......................... 177 3.3. Respuesta primaria ejercida por PhoP ante la escasez de fosfato en el medio .................................................................................. 179 3.4. Interacción de las regulaciones por carbono, nitrógeno y fósforo ...................................................................................................... 181 3.5. Efecto de PhoP en el metabolismo secundario ............................... 183 Bibliografía ..................................................................................................................... 187 4. Conclusiones ........................................................................ 195 5. Anexo ................................................................................... 199 5.1. Sitios de unión de PhoP en S. coelicolor: modelo I .......................... 199 5.2. Herramientas genéticas desarrolladas ............................................. 202 5.2.1. Construcción de los vectores sonda de promotores: pLUXAR+ y pLUXAR‐neo ................................................................................................................... 202 5.2.2. Diseño de los oligos marcados con fluorescencia, LUX‐FAM+47 y LUX‐FAM+135, para determinar el inicio de la transcripción mediante extensión de cebadores ................................................................................................. 206 Bibliografía ..................................................................................................................... 209 6. Agradecimientos .................................................................. 215 1. Introducción F. Santos Beneit 1. Introducción Este capítulo está enfocado a dar una visión general y complementar las introducciones específicas de cada uno de los artículos adjuntados. Esta introducción general se divide en dos apartados. En el primer apartado se describe la importancia del género Streptomyces como productor de metabolitos secundarios de gran interés industrial y farmacológico y la utilización de Streptomyces coelicolor como organismo modelo. En el segundo apartado se analiza la respuesta a la escasez de fosfato dependiente del regulador PhoP, esto es, el regulón pho, objeto principal de esta tesis. 1.1. Streptomyces coelicolor: organismo modelo del género Streptomyces 1.1.1. Características generales del género Streptomyces y reseña histórica del grupo de los actinomicetos Los microorganismos del género Streptomyces pertenecen al grupo de los actinomicetos.
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