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UvA-DARE (Digital Academic Repository) Ecophysiological aspects of algal host–virus interactions in a changing ocean Maat, D.S. Publication date 2016 Document Version Final published version Link to publication Citation for published version (APA): Maat, D. S. (2016). Ecophysiological aspects of algal host–virus interactions in a changing ocean. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:11 Oct 2021 Douwe Sybren Maat Ecophysiological aspects of algal host - virus interactions in a changing ocean Ecophysiological aspects of algal host - virus interactions in a changing ocean Douwe Sybren Maat Ecophysiological aspects of algal host - virus interactions in a changing ocean Douwe Sybren Maat Maat, D.S. Ecophysiological aspects of algal host – virus interactions in a changing ocean PhD thesis, University of Amsterdam Het werk voor dit proefschrift is uitgevoerd op het Koninklijk Nederlands Instituut voor On- derzoek der Zee (NIOZ), een instituut van de Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO). ISBN: 9789491407383 Graphic design cover and inside: Rachel van Esschoten, DivingDuck Design (www.divingduckdesing.nl) Printed by: Printed by: Gildeprint Drukkerijen, Enschede (www.gildeprint.nl) Ecophysiological aspects of algal host - virus interactions in a changing ocean ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit van Amsterdam op gezag van de Rector Magnificus prof. dr. ir. K.I.J. Maex ten overstaan van een door het college voor promoties ingestelde commissie, in het openbaar te verdedigen in de Agnietenkapel op vrijdag 16 december 2016, te 16:00 uur door Douwe Sybren Maat geboren te Zwolle PROMOTIECOMMISSIE Promotor prof. dr. C.P.D. Brussaard NIOZ & Universiteit van Amsterdam Overige leden prof. dr. W.H. Wilson SAHFOS, UK prof. dr. J. Huisman Universiteit van Amsterdam prof. dr. L.J. Stal NIOZ & Universiteit van Amsterdam prof. dr. G. Muijzer Universiteit van Amsterdam prof. dr. K.R. Timmermans NIOZ & Rijksuniversiteit Groningen prof. dr. S. Schouten NIOZ & Universiteit Utrecht Faculteit der Natuurwetenschappen, Wiskunde en Informatica “You are not a drop in the ocean. You are the entire ocean in a drop” -Rumi- Contents Chapter 1 General Introduction _____________________________________________________ 9 Chapter 2 Elevated carbon dioxide and phosphorus limitation favor Micromonas pusilla through stimulated growth and reduced viral impact ______________29 Chapter 3 Increasing phosphorus limitation and viral infection impact lipid remodeling of picophytoplankter Micromonas pusilla ______________________55 Chapter 4 Acquisition of intact polar lipids from the prymnesiophyte Phaeocystis globosa by its lytic virus PgV-07T ________________________________________79 Chapter 5 Fatty acid dynamics during viral infection of Phaeocystis globosa _______ 103 Chapter 6 Combined phosphorus limitation and light stress prevent successful viral proliferation in the phytoplankton species Phaeocystis globosa, but not in Micromonas pusilla _________________________________ 129 Chapter 7 Both phosphorus and nitrogen limitation constrain viral proliferation in marine phytoplankton ______________________________________________ 151 Chapter 8 Virus production in phosphorus limited Micromonas pusilla stimulated by a supply of naturally low concentrations of different phosphorus sources, far into the lytic cycle ____________________________ 177 Chapter 9 Thesis Synthesis ______________________________________________________ 207 Addendum Summary _____________________________________________________________ 218 Samenvatting _________________________________________________________ 222 Author Contributions _________________________________________________ 227 Dankwoord ___________________________________________________________ 229 Chapter 1 General Introduction Chapter 1 Phytoplankton and the abiotic environment 1 Phytoplankton are unicellular photosynthetic organisms that are suspen- ded throughout the water column and form the base of most marine pelagic food webs. In the marine environment they are accountable for approximately 48.5 Pg of inorganic carbon uptake (primary production) per year, which is roughly half of annual primary production worldwide and 98% of total pri- mary production in the marine environment (Field et al. 1998). Phytoplankton primary production varies with space and time as the result of environmental conditions. The availability of dissolved inorganic carbon (DIC) in the water column, being the substrate for primary production, affects phytoplankton production. Especially during phytoplankton blooms is DIC rapidly depleted due to rapid growth (Codispoti et al. 1982, Riebesell et al. 1993). Light in the form of photosynthetically active radiation (PAR) is the source of energy for photosynthesis and as such it is another main factor that controls phyto- plankton primary production. When the intensity of the light is too low, for example at greater depth in the water column or in waters with high turbidity (e.g. sediment load or during a dense phytoplankton bloom) phytoplankton production is severely reduced (Cloern 1999). The same holds for a reduction in the duration of the light period by mixing or seasonal changes in the win- ter season in temperate and polar regions. Alternatively, reduced availability of obligatory mineral resources for phytoplankton such as nitrogen (N) and phosphorus (P) can limit phytoplankton growth (Reynolds 2006a). Shortage of nutrients can occur during phytoplankton spring blooms in eutrophic coastal waters, whereby strong increases in phytoplankton biomass quickly deplete a specific nutrient, leading to an abrupt inhibition of growth of the dominant species (Reid et al. 1990, Cloern 1996). Under oligotrophic conditions with low nutrient concentrations (e.g. coastal summer or open ocean), phytoplankton growth depends largely on nutrients that are supplied by recycling (Harris 1986, Howarth 1988, Moore et al. 2013). As different phytoplankton species have different resource requirements, the spatial and temporal variabilities in the environment also largely determine phytoplankton size distribution and taxonomic community composition (Tilman et al. 1982, Litchman and Klaus- meier 2008, Beardall et al. 2009). The composition of phytoplankton, in turn, largely determines the structure of the pelagic food web, and herewith the ef- ficiency of carbon sequestration (Reynolds 2006b). Global change, the increase in atmospheric and oceanic CO2 and warm- ing of the earth’s atmosphere and oceans (Stocker et al. 2013), directly affects abiotic variables relevant for phytoplankton growth (Beardall et al. 2009). The atmospheric CO2 concentration increased from 300 to over 400 µatm in the last 50 years and is still rising at unceasing rate (Stocker et al. 2013). Dissolu- tion of CO2 in marine waters increases the DIC availability for phytoplankton 10 General Introduction and lowers the pH (a process called ‘ocean acidification’; Riebesell & Tortell 2011). Laboratory studies showed that not all phytoplankton species are af- 1 fected by altered CO2 concentrations. Other phytoplankton species may show changed elemental stoichiometry and increased or reduced growth rates and primary production (Riebesell & Tortell 2011; Riebesell 2004). Mesocosm ex- periments have shown net increases for smaller-sized phytoplankton groups under elevated pCO2 (Engel et al. 2008, Brussaard et al. 2013). Moreover, anthropogenic CO2 emissions are almost certainly the main cause for global warming (Stocker et al. 2013). Molecules of CO2 absorb and reemit radiation in the atmosphere, thereby trapping energy and increasing the temperature (greenhouse effect). Warming of the ocean surface will lead to an extension of temporarily and permanently vertically stratified waters (Sarmiento et al. 1998, Sarmiento et al. 2004). Phytoplankton in the mixed layer may sub- sequently experience increased nutrient limitation, because nutrient supply from deeper waters will become strongly reduced and may even be halted (Behrenfeld et al. 2006). P-limitation is particularly thought to prevail in the future oceans, because bioavailable mineral N can also be produced by N2-fix- ation (Karl et al. 1997). Furthermore, light levels in the stratified layer will be more static, yielding an environment with relatively high light levels in the rel- atively shallow mixed layer and with statically low light deeper in the euphotic zone (Finkel et al. 2010, Winder and Sommer 2012). Global change might thus affect phytoplankton community composition, growth and production in the world’s seas and oceans, with possible consequences for food web structure