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Viruses in the North Sea: Viromics and Prophage Genomics

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Viruses in the North Sea: Viromics and Prophage Genomics VIRUSES IN THE NORTH SEA: VIROMICS AND PROPHAGE GENOMICS by Alexa Garin-Fernandez a Thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Marine Microbiology Thesis Committee: Prof. Dr. Frank Oliver GLÖCKNER (chair) Alfred Wegener Institute for Marine and Polar Research Jacobs University Bremen Dr. Antje WICHELS Alfred Wegener Institute for Marine and Polar Research Prof. Dr. Matthias ULLRICH Jacobs University Bremen Dr. Gunnar GERDTS Alfred Wegener Institute for Marine and Polar Research Date of Defense: October 30, 2019 Department of Life Sciences and Chemistry, Jacobs University Bremen II STATUTORY DECLARATION Family Name, Given/First Name Garin Fernandez, Alexa Matriculationnumber 20331313 What kind of thesis are you submitting: PhD Thesis Bachelor‐, Master‐ or PhD‐Thesis English: Declaration of Authorship I hereby declare that the thesis submitted was created and written solely by myself without any external support. Any sources, direct or indirect, are marked as such. I am aware of the fact that the contents of the thesis in digital form may be revised with regard to usage of unauthorized aid as well as whether the whole or parts of it may be identified as plagiarism. I do agree my work to be entered into a database for it to be compared with existing sources, where it will remain in order to enable further comparisons with future theses. This does not grant any rights of reproduction and usage, however. The Thesis has been written independently and has not been submitted at any other university for the conferral of a PhD degree; neither has the thesis been previously published in full. German: Erklärung der Autorenschaft (Urheberschaft) Ich erkläre hiermit, dass die vorliegende Arbeit ohne fremde Hilfe ausschließlich von mir erstellt und geschrieben worden ist. Jedwede verwendeten Quellen, direkter oder indirekter Art, sind als solche kenntlich gemacht worden. Mir ist die Tatsache bewusst, dass der Inhalt der Thesis in digitaler Form geprüft werden kann im Hinblick darauf, ob es sich ganz oder in Teilen um ein Plagiat handelt. Ich bin damit einverstanden, dass meine Arbeit in einer Datenbank eingegeben werden kann, um mit bereits bestehenden Quellen verglichen zu werden und dort auch verbleibt, um mit zukünftigen Arbeiten verglichen werden zu können. Dies berechtigt jedoch nicht zur Verwendung oder Vervielfältigung. Diese Arbeit wurde in der vorliegenden Form weder einer anderen Prüfungsbehörde vorgelegt noch wurde das Gesamtdokument bisher veröffentlicht. ………………………………………………………………………………………………………………………………………… Date, Signature III IV “What is essential is invisible to the eye” Le Petit Prince (1943) V VI THESIS ABSTRACT Viruses are the most abundant biological entity on Earth, dominating the marine environment. Despite their small size, viruses have an enormous influence on microbial population dynamics, due to lysis and horizontal gene transfer. Due the high abundance of their hosts, bacteriophages or phages comprise the majority of viruses and also provide the largest reservoirs of unexplored genetic diversity in marine environments. The rise of Next Generation Sequencing (NGS) techniques brings new opportunities to investigate the marine virus community. However, there is no current statutory pipeline applied in marine phage ecology. Therefore, this thesis proposes a virus-specific pipeline based on the integration of existing tools and state of the art techniques. The developed pipeline was applied to accomplish the two research aims of this thesis: (1) to analyze the virus community in the North Sea with viromics, and (2) to characterize lysogenic phages from potentially pathogenic Vibrio species. For the first part of this thesis, the virus community of four sampling stations were described using virus metagenomics (viromics). The results show that the virus community is dominated by phages and they are not evenly distributed throughout the North Sea. In general, the coastal virus community was genetically more diverse than the open sea community. The influence of riverine inflow and currents, for instance the English Channel flow affects the genetic virus diversity with the community carrying genes from a variety of metabolic pathways and other functions. These results offer the first insights in the virus community in the North Sea using viromics and shows the variation in virus diversity and the genetic information moved from coastal to open sea areas. Although phages of emerging Vibrio species were identified in low percentage in the North Sea virome, is possible they are lysogenic phages integrated into the host genome. The seawater temperature rise promotes the growth of potentially human pathogenic Vibrio species. In the North Sea, V. parahaemolyticus and non-O1/O139 V. cholerae have been isolated and characterized. These strains contain prophages that may contribute to the emergence of pathogenic strains in the marine environment (40 % of tested isolates). The genome structure and possible biological functions of four lysogenic phages were described in the second part of this thesis. The phages from V. parahaemolyticus (two tailed phages, one filamentous phage) and V. cholerae (one tailed phages) can integrate into their host genome and might have a role in pathogenicity. This study provides new insights with respect to the presence of lysogenic phages in environmental Vibrio strains, which might have a role in the emergence of new pathogenic strains in the North Sea. This thesis represents an exemplary study of the virus community in the North Sea, with special emphasis on the marine phages. The settled virus-specific pipeline as well as the obtained insights will contribute to extend the study of the virus diversity dynamics in other marine areas, including to estimate the abundance and functional diversity of novel phages. VII VIII CONTENTS Statutory Declaration .................................................................................................................................... III Thesis abstract ............................................................................................................................................. VII Contents ..................................................................................................................................................... VIII List of Figures ............................................................................................................................................... XI List of Tables .............................................................................................................................................. XII Chapter 1 Introduction ................................................................................................................................................... 1 1.1. Marine viruses: Part of the micro-universe .................................................................................... 1 1.1.1. Marine phages and other microbial inhabitants from the North Sea ..................................... 3 1.2. the host hackers vs the time bombs: Proliferation cycle of tailed phages ...................................... 5 1.2.1. Lytic cycle, the host hackers ................................................................................................. 5 1.2.2. Lysogenic cycle, the time bombs .......................................................................................... 6 1.2.3. The viral effect: role on the ecosystem and population development .................................. 8 1.2.4. Inception of infection: Phage influence in the development of human pathogenic Vibrio strains ...................................................................................... 9 1.3. You can judge a phage by the scope it’s seen: Approaches applied in marine phage ecology ............................................................................. 11 1.3.1. Methods to collect virus biomass ........................................................................................ 12 1.3.2. Methods to estimate abundance and diversity .................................................................... 12 1.4. Methods applied to tailed phage’s characterization ..................................................................... 14 1.4.1. Methods for isolation of phage–host systems ..................................................................... 15 1.4.2. Methods to characterize morphology .................................................................................. 16 1.4.3. Methods to characterize a genome ...................................................................................... 17 1.5. NGS applied in marine virus (meta)genomics ............................................................................. 18 1.5.1. Phage (meta)genomics ........................................................................................................ 18 1.5.2. The needle in the haystack: phage genomes in the databases ............................................. 20 1.5.3. Virus (meta)genomic tools .................................................................................................. 21 1.6. Motivation and research aims ...................................................................................................... 23 1.7. Content overview ......................................................................................................................... 26 Chapter 2 North Sea
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