IMIS | Lifewatch regional portal

You are here


[ report an error in this record ]basket (0): add | show Print this page

Ecophysiological aspects of algal host: virus interactions in a changing ocean
Maat, D.S. (2016). Ecophysiological aspects of algal host: virus interactions in a changing ocean. PhD Thesis. University of Amsterdam: Amsterdam. ISBN 9789491407383. 232 pp.

Thesis info:

Available in  Author 
Document type: Dissertation

Author  Top 

    Marine phytoplankton are unicellular photosynthetic microbes that are responsiblefor roughly fifty percent of global primary production and form thebase of most of the pelagic food chains. Phytoplankton production is controlledby so called ‘bottom-up’ factors, i.e. physicochemical variables suchas light, temperature, CO2 and nutrient availability. However, phytoplanktonabundances are also regulated by ‘top-down’ mortality factors, such as zooplanktongrazing and viral lysis. Viruses are host-specific infectious particles,that consist of genetic material in a protein capsid, and which depend on hostcells to reproduce. Upon infection they replicate inside the host cell and arethen released into the extracellular environment through cell lysis, from wherethey can infect new host cells. As opposed to grazing of phytoplankton, virallysis diverts matter and energy away from higher trophic levels to the dissolvedorganic matter pool. Changes in the impact of viruses on phytoplanktonmortality might thus have subsequent impacts on food web dynamicsand biogeochemical cycling. However, despite the ecological significance of thetopic, knowledge on how the environment affects virus-phytoplankton interactionsis still largely limited. For instance, studies thus far mostly consideredthe effects of nutrient deprivation, while the possible effects of nutrient supplyrate, type of molecular compound, and the potentially interacting effect of twostressors (e.g. nutrient availability and light level) have been largely overlooked.The relevance of such studies is high as anthropogenic activities result in(i) changing nutrient load and N:P ratios, and (ii) increasing atmospheric andaquatic CO2 concentrations and warming of the surface ocean. Global warmingmay induce and/or strengthen vertical stratification which in turn leadsto a more stable light climate (high or low intensity, depending on the actualdepth) and increasing nutrient limitation.With this thesis I aimed to obtain a better understanding on how abioticfactors affect virus-phytoplankton interaction, alone and in combinationwith other relevant environmental variables. The main focus in this thesis is onphosphorus (P) limitation, for the primary reason that phytoplankton growth inmany coastal and oceanic systems worldwide is (seasonally) limited in P, and thefuture (stratified) ocean is expected to become more P-limited than nitrogen (N)limited due to diazotroph N-fixation in the ocean surface. The studies in this thesiswere carried out with axenic phytoplankton host-virus model systems underwell-controlled experimental set-ups to obtain a mechanistic understanding andallow accurate quantification of virus growth characteristics, i.e., the viral latentperiod (time until first release of viruses), the viral burst size (number of virusesproduced per host cell lysed) and the percentage of infective progeny viruses.Host cell physiology (e.g. photophysiology and lipid composition) was monitoredto relate differences in results between treatments to host metabolism.218SummaryAIn Chapter 2 of this thesis, the effects on virus-host interaction werestudied in a future ocean scenario of P-limitation with elevated partial CO2pressure (pCO2 of 750 μatm, representing the year 2100). Cells of the picoeukaryoticphytoplankter Micromonas pusilla were grown in P-limited chemostats:continuous cultures in which the growth rate (and thus the strength oflimitation) is determined by the dilution rate of the medium (0.25 μM PO43-).The P-limited cells were forced to grow at 97% and 32% of the P-replete growthrate (maximum growth rate, μmax of 0.72 d-1). At steady state (i.e. sustainedP-controlled balanced growth with constant cell abundances), the algal cellularP-quotas, photosynthetic efficiency and net primary production rateswere found severely reduced compared with the P-replete treatment. CO2 enrichmentfacilitated higher M. pusilla abundances, due to further reductionof cellular P and N quota. Upon viral infection (with M. pusilla virus MpV), ahigher CO2 concentration did not affect virus proliferation. In contrast, P-limitationled to a prolonged latent period by 3 and 6h for the 0.97 and 0.32 μmaxcultures, respectively (4-8 h under replete conditions). Moreover, the burstsize reduced 5-fold, independent of the degree of P-limitation. These resultsindicate that a combination of low P-availability and high pCO2, a likely scenariofor the future oceans, may support higher picophytoplankton biomass(elevated pCO2) and reduce their mortality by viruses (P-limitation).Chapter 3 shows that P-limitation (but not elevated pCO2) affects thecomposition of intact polar lipids (IPLs) in M. pusilla. For the first time weshow that this (i) occurs in a picoeukaryotic green alga, (ii) that the lipid remodelingdepends on the strength of limitation and furthermore (iii) that lipidremodeling can be influenced by MpV infection. The ratio of phospholipids(phosphorus containing lipids) to sulfolipids and galactolipids (sulfur- andgalactose containing lipids) was shown to strongly decrease along a gradientfrom P-replete conditions to P-controlled growth at 0.97 and 0.32 μmax, and toP-starvation. When the P-starved cultures were infected with MpV, total P-lipidsubstitution was either lower (0.97 μmax) or completely inhibited (0.32 μmax).Thus the effects of viral infection on the IPL composition were dependent onthe growth history of the cells. This study demonstrates that not only P-concentration,but also the P-supply rate can affect phytoplankton lipid composition,and that viral action can interfere with host lipid metabolism and as suchaffect the chemical composition of dissolved and particulate organic matter.The effect of viral infection on host IPL composition was further investigatedfor the haptophyte Phaeocystis globosa (Chapter 4). Viral infection of P.globosa with its virus PgV did not lead to changes in IPL composition. This isin itself remarkable because literature shows that lipid profiles of the closelyrelated haptophyte Emiliania huxleyi are strongly affected by viral infection.A closer look to the IPL bound fatty acids (FAs; Chapter 5), however, revealsthat viral infection did lead to a decrease of polyunsaturated FAs. Organisms219SummaryAin higher trophic levels are dependent on phytoplankton for these highly nutritionalcompounds and hence these results suggest that viral infection ofP. globosa has the potential to affect ecosystem dynamics by reducing theavailability of PUFAs in the system (via grazing on infected cells or via lyseddissolved organic matter). Chapters 3, 4 and 5 furthermore describe that MpVand PgV possess lipid membranes, which resemble host lipid composition,but that they are impoverished in thylakoid membrane specific galacto- andsulfolipids. The profile of PgV showed shorter and more saturated FAs thanthe average FAs of the host. Both viruses might selectively recruit their membranesfrom their phytoplankton host, i.e. from specific cell compartments.In Chapters 6 and 7 the effects of P-limitation on M. pusilla and P.globosa were investigated in relation to light availability and N-limitation, respectively.Chapter 6 shows that P-limitation in combination with relativelylow or high light level (respectively 25 and 250 μmol quanta m-2 s-1) resultedin severely reduced photosynthetic efficiencies for both phytoplankton species(compared to medium light level of 100 μmol quanta m-2 s-1 and the P-repletetreatment). The low and high light treatments did not affect virus proliferationin infected M. pusilla. In contrast, the viral burst size of PgV decreased by 55and 23%, respectively. Remarkably, only 2 and 4% of the virus progeny wereinfective, as compared to 62% for P-limited under standard light level. Thisstudy clearly shows that light level can drastically strengthen the negative effectsof P-limitation on virus infectivity and that this effect is host species-specific.Simultaneously low availability of P and N (Chapter 7) did not lead tosuch cumulative constraints on viral proliferation in M. pusilla and P. globosa.Although for both species the steady state maximum growth rate under NandNP-limitation was equal to P-limitation, the NP-limited treatment showedmost resemblance to the N-limited cultures in mean cell size, cellular meanchlorophyll fluorescence, and photosynthetic efficiency. All infected N- andNP-limited cultures showed similarly prolonged viral latent periods as underP-limitation. While MpV burst sizes were equally reduced under N- andP-limitation (i.e. ±70%), the burst sizes of PgV were further reduced by 94%under N- and NP-limitation (as compared to 70% for P-limitation). The resultsdemonstrate that N-limitation can be equally inhibiting or be an even strongerinhibitor of viral proliferation than P-limitation. This is in shear contrast to thethus far prevailing perception that algal virus production is hardly affected byhost N-limitation.The previous chapters indicate that the availability of P is an importantregulating factor of algal virus proliferation and that the outcome of infectiondepends on the strength of the metabolic limitation of the host prior to infection(i.e. the supply rate of P). The latter is an important finding as primaryproducers in seas and oceans experience different degrees of P-limitation.220SummaryAFurthermore, primary production in oligotrophic pelagic systems dependsstrongly on a continuously low supply of nutrients by nutrient recycling. Itherefore studied the effect of near-continuous supply of the limiting nutrient(i.e. P) to infected M. pusilla (Chapter 8). A low supply of the soluble reactive P(SRP) to P-limited M. pusilla during the infection cycle resulted in a doublingof the burst size as compared to no addition, independent of the level of P-limitation(0.97 or 0.32 μmax). Delaying this supply up to 18h post infection stillincreased the burst size to a similar level. Supply with an organic P-source(soluble non-reactive P, SNP) led to a similar burst size stimulation as withSNP, illustrating efficient utilization of SNP compounds by M. pusilla duringinfection. Viral burst sizes were even stimulated by natural SNP in virus-freelysate (also SRP-free) of previously lysed P-limited M. pusilla. This study showsthe importance of the supply rate of ecologically relevant low concentrations ofP for virus production in P-limited phytoplankton hosts. The data suggest thatremineralization (illustrated by the SRP-supply) and viral lysis of neighboringcells (mimicked by the SNP treatment) can promote viral proliferation andthus phytoplankton mortality by viral lysis even though SRP concentrationsin the water are depleted.Overall, the research presented in this thesis provides new insights intohow the type and level of nutrient limitation determines the outcome of thelytic virus infection of phytoplankton-hosts. Moreover, depending on the species,light level can force an additional constraint on already relatively lowviral burst sizes of nutrient-limited phytoplankton. The success of lytic viralinfection (speed of production and number of produced viruses) is thus dependenton the metabolic state of the host cells and variability in environmentalfactors has a strong potential to influence virus production and subsequentlyviral-induced phytoplankton mortality. No direct role for IPLs and FAs inthe interaction between the physicochemical environment and phytoplanktonproliferation was observed, but viral infection was found to have the potentialto interfere with how the environment affects host IPL composition, possiblyaltering the nutritional (FA) value of phytoplankton. Knowledge on how theenvironment affects phytoplankton viral lysis becomes more important as thehuman population drastically influences the earth’s atmosphere and oceans.This thesis strengthens the hypothesis that virus activity and viral-inducedphytoplankton mortality might be strongly affected by global change processes,with consequent potential effects on food web dynamics and biogeochemicalcycling. Further study, in line with this thesis, is needed to investigate theeffects of the environment on virus-host interaction, with particular emphasison differences between host species, virus strains infecting the same species,and examination under natural conditions.

All data in the Integrated Marine Information System (IMIS) is subject to the VLIZ privacy policy Top | Author