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Gran-Stadniczenko~ A, Elianne Eggea, Vladyslava Hostyevab, Ramiro Logaresc, Wenche Eikrema,B & Bente Edvardsena a Department of Biosciences, University of Oslo, P

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Gran-Stadniczenko~ A, Elianne Eggea, Vladyslava Hostyevab, Ramiro Logaresc, Wenche Eikrema,B & Bente Edvardsena a Department of Biosciences, University of Oslo, P DIVERSITY AND COMMUNITY DYNAMICS OF PROTISTS AND THEIR VIRUSES IN THE SKAGERRAK Sandra Gran Stadniczeñko Dissertation presented for the degree of Philosophiae Doctor (PhD) 2019 Section for Aquatic Biology and Toxicology Department of Biosciences Faculty of Mathematics and Natural Sciences University of Oslo © Sandra Gran Stadniczeñko, 2019 Series of dissertations submitted to the Faculty of Mathematics and Natural Sciences, University of Oslo No. 2097 ISSN 1501-7710 All rights reserved. No part of this publication may be reproduced or transmitted, in any form or by any means, without permission. Cover: Hanne Baadsgaard Utigard. Print production: Reprosentralen, University of Oslo. “With every drop of water you drink, every breath you take, you're connected to the sea. No matter where on Earth you live.” Sylvia A. Earle To my Mom To my family ACKNOWLEDGEMENTS First and foremost, I would like to thank Prof. Bente Edvardsen. Thank you, Bente, for giving me the opportunity to do this PhD, for your mentorship and all your help in the devel- opment of this thesis. Also, to my co-supervisors Wenche Eikrem, Tom Andersen and Josefin Titelman, for your additional inputs, especially Josefin for your comments and encouragements when it got really difficult. This thesis was possible due to the financial support from the Research Council from Nor- way through the HAPTODIV and MICROPOLAR projects. I would also thank the BioMarKs project that provided for some of the samples, and ASSEMBLE for funding for the research stay. A special thanks to Elianne D. Egge, my predecessor in the PhD. If you did not take all those samples, I wouldn’t have had anything to work from. I also want to thank you for all your patience and knowledge during our time together at the office when I needed it. Sissel Brubak, thank you for your help in the laboratory when I was not able to process the samples and to Rita Amundsen for assistance during samplings. Thank you both, and Berit Kaasa, for all the morning talks in the lunch room that made easy the start of each day. Jan Heuschele… I do not have enough words to thank you for all your support both in statistics and personally. You did not only save my data when I got stuck with R a million times, but you were always there when I had a bad day, and I really appreciate it. I wish you all the best for the future; you deserve it. To my AQUA colleagues Luka, Elisabeth, Marcin, Raoul, Torben, Fran, Roul, Daniel, Lina, Maryia, Zhanna and especially Andrea, some of you already away from UiO, but I loved our chats at the lunch room which made the days better. Andrea, I made it! And you will too!!! Luka, Ramiro and Anders for your collaborations in my thesis work. I learned a lot form all and each one of you, microscopy… bioinformatics…phylogenies… which are of primary importance in this thesis. The biggest thanks to my friends and family which were a great support during this PhD. And thus, I will address them in their languages. I Fran Lu, ni te imaginas lo importante que has sido en esta época de subidas y bajadas. Gracias por tu apoyo a diario cuando todo iba bien o mal. ¡Tú mismo pasaste por lo mismo y has sabido animarme cuando ya estaba al límite. Me siento muy afortunada de tenerte como amigo y, para qué mentir, ¡como un hermano! te luvo mucho! Diana, Isa, Tania, Paloma, Vane, Marta, Almu… Tantos amigos que dejé al venirme a Oslo y que seguís ahí a pesar de la distancia. Muchas gracias a todos por vuestro apoyo. Me siento muy orgullosa de teneros! Årul Jørgensen and Ana Martínez muchísimas gracias por vuestra ayuda sobre la lengua inglesa de último momento! Johann, mon amour, merci pour tout ton support et pour m'avoir donné nos fils Julia et Liam. Ils sont le meilleur cadeau que j’ai jamais eu. Vous êtes ce qui me fait sourire chaque jour. Merci beaucoup pour ta patience et pour tous les moments qu'on a vécu ensemble. Je t'aime. Julia y Liam, mis dos amores. Gracias por haber aparecido en mi vida. Sois lo que me hace seguir adelante en cada momento, la alegría de mis días. Os quiero muchísimo. A mi familia, papa, Timur y Roci. Por estar siempre allí, por apoyarme en mi decisión para estudiar Ciencias del Mar. Por empujarme a perseguir mis sueños y dejar el nido. Por seguir ahí en los buenos y malos momentos, sobre todo estos últimos meses tan duros para todos nosotros, os quiero. Babciu i ciociu, bardzo wam dziękuję za wsparcie w ciągu tych ostatnich lat, w szcze- gólnie w tych ostatnich trudnych miesiącach. Mamo… Dziekuje ci za wszystko. Nie masz pojęcia, jak bardzo za tobą tęsknię. Od- szedłaś w momencie kiedy najbardziej cię potrzebowałam. Mam nadzieję że jesteś ze mnie dumna, gdziekolwiek jesteś. Kocham cię bardzo. Oslo, November 2018 Sandra Gran Stadniczeñko II TABLE OF CONTENTS % ' !! !! !" !$ !& !) "! "# "' !( #! III IV SUMMARY Marine coastal areas are among the most productive ecosystems in the world. Protists play key ecological roles in these systems, and it is thus essential to characterise who the main players are. Yet, eukaryotic microbial diversity in marine habitats, especially the smaller nano- and picoplankton, is still poorly described and under-sampled. The main theme of my thesis is to reveal the diversity and dynamics of protists and their viruses by molecular methods in the Outer Oslofjorden, Skagerrak. This work was also the first to perform studies on both the protist diversity and seasonal patterns and their co-occurrent viruses in Norwegian coastal waters by high-throughput sequencing (HTS, 454-pyrosequenc- ing) throughout two-years (2009-2011). We also aimed to test the 18S and 28S rRNA marker genes to study the haptophyte plankton community and to compare the application of high- throughput sequencing HTS with the scanning electron microscopy method for analysis of the coccolithophore community. Further, we wanted to improve the knowledge about the ichthyo- toxic species in the Skagerrak. Our results have revealed a higher richness of protists and algae-infecting viruses compared to previous surveys carried out for more than a decade in the Skagerrak. This demonstrates that a vast diversity remains to be described both morphologically and genetically. We also revealed which species dominate in the HTS and found taxa not previously recorded in the area by microscopy or taxa novel to science. Further, we provided a curated 28S rRNA gene reference database based on cultures, contributed to linking molecular and morphological data and 28S to 18S rRNA gene sequences without cultured representatives and also improved the metabar- coding methodology. Our studies may serve as a baseline for future surveys and monitoring of planktonic communities to understand the effects of environmental and climate changes. 1 2 LIST OF PAPERS This thesis is built upon the following four original research papers, which will be referred to in the text by their Roman numerals: I. Gran-Stadniczeñko, S., Egge, E. D., Hostyeva, V., Logares, R., Eikrem, W. & Ed- vardsen, B. (2018). Protist Diversity and Seasonal Dynamics in Skagerrak Plankton Communities. Journal of Eukaryotic Microbiology. https://doi.org/10.1111/jeu.12700 II. GranStadniczeñko, S.*, Šupraha, L.*, Egge, E. D., & Edvardsen, B. (2017). Hapto- phyte diversity and vertical distribution explored by 18S and 28S ribosomal RNA gene metabarcoding and scanning electron microscopy. Journal of Eukaryotic Microbiol- ogy, 64(4), 514-532. * These authors contributed equally III. Engesmo, A., Strand, D., Gran-Stadniczeñko, S., Edvardsen, B., Medlin, L. K., & Eikrem, W. (2018). Development of a qPCR assay to detect and quantify ichthyotoxic flagellates along the Norwegian coast, and the first Norwegian record of Fibrocapsa japonica (Raphidophyceae). Harmful Algae, 75, 105-117. IV. Gran-Stadniczeñko, S., Krabberød A. K., Egge, E. D., Yau, S., Sandaa R. A. & Edvardsen, B. Seasonal dynamics of algal infecting viruses in the Skagerrak, North Atlantic and inferred interactions with protists. Manuscript. Papers I-III and Figure 2 are re-printed with the permission of the publishers. 3 4 INTRODUCTION Marine protists and their ecological importance Marine coastal areas are among the most productive ecosystems in the world. About 33% of the total marine biomass is formed by protists (Bar-On et al. 2018). Protista is an extremely diverse and paraphyletic group of mostly unicellular microeukaryotes, but there are numerous colonial and multicellular taxa. Highly abundant in the euphotic zone, protists play an essential role with diverse ecological functions (Figure 1), and it is thus important to characterise who the main players are (del Campo et al. 2016). Protists: i) serve as the base of marine food webs (Cushing 1989; Massana et al. 2006), ii) influence the productivity and stability of ecosystems across trophic levels (Ptacnik et al. 2008) and, iii) affect the ability of the ocean to function as a natural carbon sink by fixing CO2 (e.g. De La Rocha and Passow 2007). The grazing activity of heterotrophic protists, together with marine viruses, makes them important control agents of nano- and picoplankton, maintaining populations at relatively stable concentrations in oceanic systems (Suttle 2005; Logares et al. 2012; Prowe et al. 2012). For example, Maar (2003) showed that the grazing impact of ciliates and heterotrophic dinoflagellates in the spring blooms in Skagerrak exceeded that of copepods with a factor of 3 to 4. The species composition and the relative abundance of the different taxa present in plank- ton communities undergo seasonal changes, which are of major importance in the coupling between primary producers and higher trophic levels. Identifying the mechanisms that shape marine protist communities has been a centre of interest for researches in the past years.
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