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Viruses in the Marine Environment 2014 Elena Lara de la Casa Casa la de Lara Elena community dynamics, phage-host interactions and genomic structure. genomic and interactions community dynamics, phage-host phage-host dynamics, community interactions and genomic structure. Elena Lara de la Casa, Enero 2014 UNIVERSIDAD DE LAS PALMAS DE GRAN CANARIA Departamento de Biología D/Dª José Manuel Vergara Martín SECRETARIO DEL DEPARTAMENTO DE BIOLOGÍA DE LA UNIVERSIDAD DE LAS PALMAS DE GRAN CANARIA, CERTIFICA, Que el Consejo de Doctores del Departamento en su sesión de fecha.............................tomó el acuerdo de dar el consentimiento para su tramitación, a la tesis doctoral titulada “Viruses in the marine environment: community dynamics, phage-host interactions and genomic structure” presentada por el/la doctorando/a D/Dª Elena Lara de la Casa y dirigida por las Doctoras Dolors Vaqué y Silvia González Acinas. Y para que así conste, y a efectos de lo previsto en el Artº 6 del Reglamento para la elaboración, defensa, tribunal y evaluación de tesis doctorales de la Universidad de Las Palmas de Gran Canaria, firmo la presente en Las Palmas de Gran Canaria, a...de....................................de dos mil............ 3 Viruses in the marine environment: community dynamics, phage-­‐host interactions and genomic structure (Los virus en los ecosistemas marinos: dinámica de la comunidad, interacciones entre fago y hospedador y estructura genómica) Elena Lara de la Casa Tesis Doctoral presentada por Dª Elena Lara de la Casa para obtener el grado de Doctor por la Universidad de las Palmas de Gran Canaria, Departamento de BiologFa, Programa en GceanograHFa (Bienio 2008-­‐2010) Directores: Dra. Dolors Vaqué y Dra. Silvia G. Acinas Universidad de las Palmas de Gran Canaria Institut de Ciències del Mar (ICM-­‐CSIC) La Doctoranda El director El Co-­‐director Elena Lara de la Casa Dolors Vaqué Silvia G. Acinas En Barcelona, a de de 2014 5 This thesis has been funded by the Spanish Ministry of Science and Innovation (MICINN) through a PhD fellowship to Elena Lara de la Casa, under the program “Formación de Personal de virus que infectan a microorganismos marinos-MICROVIS” (Ref. CTM2007-62140/MAR, P.I.Dr Investigador (FPI)”, and was ascribed to the project: “Aislamiento, identificación y especificidad Dolors Vaqué). Other projects that contributed partially to the completion of this thesis were: “Population Ecology of Model Marine Heterotrophic Flagellates–FLAME” (CGL2010-16304, funded by the MICINN, P.I. Dr. Ramón Massana), “Arctic tipping points-ATP” (contract #226248 in the FP7 program of the European Union, P.I.: P.F. Wassman. University of Tromso, (Norway), and P.I. from CSIC, C.M. Duarte. IMEDEA), “The Role and Mechanisms of Genomic Microbial Microdiversity: a perspective integrating genomics and ecological approaches-MICRODIVERSITY” (CGL2008-00762/BOS, funded by the MICINN, P.I. Dr. Silvia G. Acinas) and “Microbial Ocean Pangenomes: from single cell to bacterial population genomics–PANGENOMICS” (CGL2011-26848/BOS, funded by the MICINN, P.I. Dr. Silvia G. Acinas) and. 7 A mis padres. 9 CONTENTS Abstract /Resumen/Resum 13 List of Publications 17 General Introduction 21 Aims and Outline 37 Chapter 1 Absence of seasonality on viral dynamics and salinity as a main driver modulating viral abundance in the NW Mediterranean Sea 43 Chapter 2 Experimental evaluation of the warming effect on viral, bacterial and protistan communities in two contrasting Arctic systems 77 Chapter 3 Pseudoalteromonas sp. 109 phages Marine phage-bacteria interactions at fine-scale within Chapter 4 Life-style and mosaic genome structure of marine Pseudoalteromonas siphovirus B8b isolated from the Northwestern Mediterranean Sea 141 Chapter 5 Comparative genomics and biogeography of Pseudoalteromonas phages 177 Synthesis of results and general discussion 197 Resumen en español/Spanish Summary 213 References (Introduction, Discussion and Spanish summary) 255 Agradecimientos/Acknowledgments 271 11 ABSTRACT There are an estimated 1030 viruses in the world oceans, the majority of which are phages of marine phages on microbial abundance, community structure, genetic exchange and global (viruses that infect bacteria). Extensive research has demonstrated the significant influence biogeochemical cycles. In this thesis, we contribute to increase the knowledge about the ecological role of viruses in marine systems, but also we aimed to provide a better understanding about the interactions between phages and their hosts and the genetic pool and biogeography of some the isolated phages genomes. Firstly, we followed the seasonal variability of viral communities in a coastal marine site (Blanes Bay Microbial Observatory, BBMO) and the environmental and biological factors that could modulate them. Our results showed that viral communities did not follow any clear seasonal patterns during the 5 years studied period and that viruses were mainly negatively correlated with salinity. Secondly, given the actual concern of the climate change effects on marine ecosystems, we evaluated experimentally how increasing temperatures would affect the microbial loop via protists respect to via viruses (“viral shunt”) in two contrasting Arctic marine systems. Lytic life strategy dominated instead the lysogenic strategy when we increased the temperature. But, overall the most important factor controlling bacterial abundance was bacterivory. These two studies provide us a general overview regarding viral dynamics at the community level but without knowing who infects whom and who is doing what. To provide inputs into these relevant issues, we used the model of Pseudoalteromonas bacterial strains and its phages. Our results suggest that interactions between phages and hosts are highly complex in terms on infectivity and rank reaching to the family boundaries. marine phages are unrepresented susceptibility at microdiversity level but Pseudoalteromonasalso reflect that phages can infect at larger taxonomic with only 4 genomes public available. Therefore, one of the isolated Pseudoalteromonas phage from BBMO was deeply studied; we investigated its biology, morphology, genomic and proteomic characteristics. Moreover, we carried out a genomic comparison of 3 Pseudoalteromonas phages isolated from the same bacterial specie to get insights into the genome structure and functional diversity. The genomic data analyzed not only contributed to a better understanding of phage- host interactions in marine systems but also demonstrated the complexity of their dynamics and biogeographic patterns. 13 RESUMEN Se estima que hay 1030 virus en los océanos, la mayoría de los cuales son fagos (virus que infectan en la abundancia microbiana, la estructura de la comunidad, el intercambio genético y los ciclos bacterias). Numerosas investigaciones han demostrado la gran influencia de los fagos marinos biogeoquímicos globales. En esta tesis, dividida en cinco capítulos, no solo se contribuye a aumentar el conocimiento sobre el papel ecológico de los virus en los sistemas marinos, sino que también se quiso proporcionar una mejor comprensión de las interacciones entre los fagos y de fagos aislados. Para indigar sobre el papel ecológico de los virus en relación a su abundancia, sus hospedadores, la variedad genética de los virus y la biogeografía de algunos de los genomas en el primer capítulo estudiamos la variabilidad estacional de las comunidades virales en una zona costera y los factores ambientales y biológicos que podrían modular su dinámica. Nuestros resultados mostraron que las comunidades víricas no siguen ningún patrón estacional claro durante los 5 años del período estudiado y se detectó una correlación inversa entre la abundancia vírica y la salinidad. Dada la actual preocupación de los efectos del cambio climático en los ecosistemas marinos, en el segundo capítulo se evaluó experimentalmente cómo el aumento de las temperaturas afectarían al bucle microbiano a través de los protistas (“grazing”) respecto a la “viral shunt” (a través de los virus) en dos sistemas marinos del Ártico. El mecanismo de infección que dominó cuando aumentamos la temperatura fue la lisis en vez de la lisogenia. Sin embargo, el factor más importante que controlaba la abundancia bacteriana era la bacterivoría. En estos dos primeros capítulos el objetivo era tener una visión general con respecto a la dinámica viral a nivel de comunidad, aunque sin saber quién infecta a quién y quién está haciendo qué. Para proporcionar nuevo conocimiento sobre este campo, en el tercer capítulo se utilizó un modelo basado en cepas bacterianas de Pseudoalteromonas y fagos aislados de estas cepas. Nuestros resultados sugirieron que las interacciones entre fago y hospedador son altamente complejas en que los fagos pueden infectar en un mayor rango taxonómico de lo descrito actualmente términos de infectividad y susceptibilidad a nivel de microdiversidad, pero también reflejaron ya que pueden llegar a infectar cepas bacterianas de diferente familia. Los fagos marinos de Pseudoalteromonas están representados únicamente con 4 genomas públicos disponibles. Así pues en el cuarto capítulo nos centramos en el estudio de uno de los fagos de Pseudoalteromonas que aislamos. Investigamos sus características biológicas, su morfología, la genómica y la proteómica. Finalmente, en el quinto capítulo, se realizó una comparación genómica de 3 fagos aislados de Pseudoalteromonas de la misma especie bacteriana para entender mejor la estructura de los genomas y la diversidad funcional. Los datos genómicos analizados
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