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2 Tesis IDUS Embargo 12 Me Cover. Co-expression network of transcripts of Nostoc sp. PCC 7120 with expression changes after removal of combined nitrogen (left). 3D structural model of sRNAs Yfr1 (top right) and NsiR1 (bottom right). Models were generated by RNAComposer (Popenda et al. 2012. Nucleic Acids Research, 40: e112. doi: 10.1093/nar/gks339). Instituto de Bioquímica Vegetal y Fotosíntesis Departamento de Bioquímica Vegetal y Biología Molecular Universidad de Sevilla - Consejo Superior de Investigaciones Científicas TESIS DOCTORAL Global identification of regulatory RNAs in the cyanobacterium Nostoc sp. PCC 7120. Functional characterization of Yfr1 and NsiR1. Trabajo presentado por Manuel Brenes Álvarez para optar al grado de Doctor Manuel Brenes Álvarez, Sevilla, 2019 Director Directora Dr. Agustín Vioque Peña Dra. Alicia María Muro Pastor Catedrático de la Universidad de Sevilla Científica Titular del Consejo Superior de Investigaciones Científicas FUNDING This Doctoral Thesis has been carried out at the Instituto de Bioquímica Vegetal y Fotosíntesis (IBVF, CSIC-US) and has been funded by a FPU predoctoral contract from Ministry of Education, Culture and Sport (FPU014/05123). The work has been funded by projects from Ministry of Economy and Competitiveness (BFU2013-48282-C2-1-P, Non-coding RNAs involved in adaptation to nitrogen stress and cell differentiation in cyanobacteria) and from State Research Agency, Ministry of Economy, Industry and Competitiveness (BFU2016- 74943-C2-1-P, Participation of non-coding RNAs in regulatory circuits controlled by nitrogen availability in cyanobacteria) whose Principal Investigator was Dr. Alicia María Muro Pastor. Both projects were co-financed by the European Regional Development Fund (ERDF). In addition, a three-months stay at the laboratory of Dr. Wolfgang Hess (University of Freiburg, Germany) was funded by a fellowship from Ministry of Education, Culture and Sport (EST16/00088). A mis abuelos AGRADECIMIENTOS En primer lugar, me gustaría agradecer a mis directores, Agustín y Alicia, su paciencia y dedicación en estos años que hemos trabajado juntos. Su pasión por la Ciencia y su constante atención han sido una inspiración y un importante apoyo a lo largo de esta tesis. Al Dr. José Enrique Frías, por su experta ayuda durante la realización de los ensayos de actividad de nitrato y nitrito reductasa. A la Dra. Iris Maldener y la Dra. Rebeca Perez por su ayuda en las tinciones de peptidoglicano naciente. I would like to thank Dr. Wolfgang Hess for allowing me to stay for three months in his laboratory in Freiburg. Thank you for being so kind and helpful, making me feel like home there. Gracias a toda mi familia por su inmenso cariño y apoyo. A mis abuelos, por enseñarme que con trabajo, constancia y esfuerzo todo se consigue. A mis padres, porque sin su educación e inmensa confianza probablemente esta tesis no habría tenido lugar. A mi hermana Mercedes, porque su valentía para enfrentarse a nuevos problemas siempre ha sido un motivo de inspiración. A mis compañeros de laboratorio, Isidro y Elvira, por su ayuda y por hacer mucho más ameno todo mi tiempo en el laboratorio. A Javi, Alejandro, Mari, Diego, Tommy y muchos otros compañeros, por no ser sólo compañeros de trabajo, sino también buenos amigos con los que salir, charlar, desconectar del trabajo y, en resumen, disfrutar de la vida. Por último, quisiera darle las gracias a Ana por apoyarme en todo lo que hago. Gracias por escucharme detenidamente cuando comento mis tribulaciones científicas, incluso aunque el tema te sea completamente desconocido y gracias por enseñarme cómo no debo dejarme abrumar por los problemas. Finalmente, gracias a todas aquellas personas que de un modo u otro han influido en mi desarrollo como persona y en la consecución de este trabajo de tesis. We ought not to hesitate nor to be abashed, but boldly to enter upon our researches concerning animals of every sort and kind, knowing that in not one of them is Nature or Beauty lacking. Aristotle. Parts of animals, I. INDEX INDEX 1. INTRODUCTION ............................................................................................................... 1 1.1 The cyanobacteria .......................................................................................................... 3 1.1.1 General characteristics ...................................................................................................... 3 1.1.2 Cyanobacterial cell envelope ............................................................................................. 7 1.1.2.1 Synthesis and remodeling of peptidoglycan ................................................................ 7 1.1.2.2 Transporters ................................................................................................................. 9 1.1.3 Metabolic characteristics ................................................................................................. 10 1.1.3.1 Carbon assimilation in cyanobacteria ........................................................................ 11 1.1.3.2 Nitrogen assimilation in cyanobacteria ..................................................................... 11 1.1.4 Adaptation to combined nitrogen deprivation ............................................................... 15 1.1.4.1 General response ....................................................................................................... 15 1.1.4.2 Heterocyst differentiation.......................................................................................... 16 1.2 RNAs regulators in bacteria .......................................................................................... 20 1.2.1 Types of RNA regulators .................................................................................................. 23 1.2.1.1 RNA regulators encoded in cis ................................................................................... 23 1.2.1.2 RNA regulators encoded in trans ............................................................................... 24 1.2.2 Identification of RNA regulators and their targets .......................................................... 27 1.2.3 RNA regulators in cyanobacteria ..................................................................................... 28 1.2.3.1 Identification of RNA regulators in cyanobacteria ..................................................... 28 1.2.3.2 Physiological processes regulated by RNA regulators in cyanobacteria .................... 29 2. OBJECTIVES.................................................................................................................... 33 3. SUMMARY OF RESULTS .................................................................................................. 37 3.1 CHAPTER I: A computational approach for the identification of conserved sRNAs in heterocyst-forming cyanobacteria........................................................... 45 3.2 CHAPTER II: Yfr1, a widely conserved sRNA, regulates the integrity of the cell wall and its remodeling during heterocyst differentiation .................................. 67 3.3 CHAPTER III: A co-expression network to dissect the complex transcriptome of Nostoc sp. PCC 7120 during heterocyst differentiation............................. 103 3.4 CHAPTER IV: NsiR1, a sRNA with multiple copies, regulates heterocyst differentiation . 157 4. GENERAL DISCUSSION .................................................................................................. 209 5. CONCLUSIONS ............................................................................................................. 221 6. GENERAL REFERENCES ................................................................................................. 225 i 1. INTRODUCTION Introduction 1. INTRODUCTION 1.1 The cyanobacteria 1.1.1 General characteristics Cyanobacteria are Gram-negative bacteria that form a monophyletic group inside the eubacteria (Woese, 1987). They are photosynthetic microorganisms with a photosynthetic apparatus similar to that of chloroplast of algae and higher plants (DeRuyter and Fromme, 2008) and are the only prokaryotes able to perform oxygenic photosynthesis. Nowadays, it is widely accepted that chloroplasts from algae and higher plants have evolved from ancient cyanobacteria that established a symbiotic relationship with a phagotrophic eukaryote (Margulis, 1975; Ochoa de Alda et al., 2014). However, there are some differences between the photosynthetic apparatus of cyanobacteria and algae and those of higher plants. For example, in contrast to algae and higher plants, most cyanobacteria do not have chorophyll b (Stanier and Cohen-Bazire, 1977) and contain phycobilisomes as supramolecular light-harvesting complexes (Grossman et al., 1993b). Cyanobacteria played a crucial role in Earth’s history. They are thought to be the first organisms that performed an oxygenic photosynthesis (Buick, 1992). The oldest cyanobacterial fossils were found in sedimentary rocks generated more than 3500 million years ago (Schopf and Packer, 1987) and, although with some controversy, it is now accepted that these first photosynthetic organisms may have appeared between 2350 (Kirschvink and Kopp, 2008) and 3600-3700 million years ago (Garcia-Pichel et al., 2019). The ability to use water as electron donor, and the production of oxygen as a result, contributed to one of the most drastic changes in the Biosphere, the change from an anoxygenic atmosphere to an oxygenic atmosphere, a process known as the Great Oxidation Event
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