van Oijen, Tim

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   University of GroningenIron and light limitation of carbohydrate production by phytoplankton in the Southern Oceanvan Oijen, TimIMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.Document VersionPublisher's PDF, also known as Version of recordPublication date:2004Link to publication in University of Groningen/UMCG research databaseCitation for published version (APA):van Oijen, T. (2004). Iron and light limitation of carbohydrate production by phytoplankton in the SouthernOcean. s.n.CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license.More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne-amendment.Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.Download date: 06-06-2022SUMMARYSummaryThe Southern Ocean is a net sink of carbon dioxide (CO:). nowadavs considered as themajor greenhouse gas. This apparent sink function is remarkable because the SouthernOcean is i i  majclr uprvell ing area wherc cleep wate rs with high COr content are brclught crthe surface. Howcver, these deep waters are alscl righ in essential major nutrients (such asnitroscn and phosphi'rrus) supporting fixation of CO2 by phytoplankton. Part of theph<ltosynthcticallv f ixecl carbon in surface waters is exported to the deep sea by the sinkingof phytoplankton cells or aggregatcs, er nrechanisnr often rcferred to as the 'biologicalpunlp'. This leads to undersatrrration of COz irr the surface waters and, consequently,uptake of COz from the atmosphere.However, phytoplankton in the Southern Ocean do not always Íully uti l ise the majornutrients that are available to them. In large parts of this ocean province, highconcentrations ol these nutrients remain in the surface waters in association with lowstanding stocks of phytoplankton. Shipboard irnd ín situ iron addition experiments havedernonstrated that in these regions insufficient iron availabil i$, l imits phytoplanktongrowth. Iron is involved in many processes insicle phytoplankton cells. It is of crucialimportarrce for photosvnthesis. because iron-sulphur clusters facil i tate the transport ofelectrons in the photosynthetic rnembranes of thc clrkrroplasts. Also, the iron-containingcnzyme fèrredoxin is needed Íbr the gencration of reducing power. Finallv, iron is acomponent of enzymcs involved in the nitrogen mctabolism.Ncxt to iron, other factors including temperature and light are known to controlphytoplankton productivitv in the Southern Occan. This thesis was wlittcn to get a betterunderstanding of the relative impact of iron and light l imitation on Antarctic phyto-plankton growth. The research focused on the production of storage carbohydrates. Thesecarbohydrates accumulate in phytoplankton cells at high l ight levels. They are subsequentlyrespired when light availabil itv is low to supply energy and carbon skeletons tbr continuedprotein synthesis. Storage carbohydrates are considered tcl be essential for phytoplanktonso they can grow fast in a dynamic l ight enviror.rment. A variable l ight climate is tvpical ofthe Southern Ocean where deep wind-induced mixing is the rule rather than the exception.The short-term dynamics in storage carbohydrates, a major part of rvhich is water-extractable, have hardly been studied for natural pelagic phytoplankton populations so far.r59SUMMARYThe rrrairt qucstions addressccl in this thesis rvcrc:o Do wuÍar-extru(toltlc curboh-ytlrut(s suit tt.s short-Ícnrt ,stotuee protlu(t,\ itt .4nÍurcticpltvtt4tlurtkton?o llltut is the ef't'ec't o.f irott limitutiott on tha curboltytlrute nrctubolisnt o.l'Antordicpltytoplottkton?. Hrtx' i.s tlis c.ffa<'t in.llLrt'ttcatl by ligltt utttlitiott.s?Various approaches have bccn used to answer these qucstions: laboratory cultureexpcriments, shipboard incubation expcriments with natural phytoplankton populations, i l,r l/rr measurcmcnts, and an lzl . i i lrr iron enrichmcnt experiment. The field expcrimentsextencled thc knowledge of thc scasonal and rcgiclnal variations in the rel:rt ive rolc of ironand othcr  factors.  especia l lv  l ight .  in  l imi t ing phytoplankton src l rv th in  the Southern Ocean.At thc start of the projcct a method was developed lor the measurenrcnt of storagepolvsaccharidcs. Based on the che mical propertics of glucan, thc most abundant storagepolysaccharide in phytoplankton, a hot-water-extraction of particulate matter was used tctsepílrate storagc polysaccharidcs fronr structural ancl mucus polysacchirridcs. Thepolysaccharidc concentri lt ion in thc extÍi lct rvas analysed using thc TPTZ (2.1.6.-tripyridyl-s-triazine) rnethocl.Do water-extractable carbohydrates serrle as short-term storage products in ,4ntarcticphytoplankton?The amount of water-ertractablc polysaccharidcs exhibited strong day-night variations incultures of the Anttrctic diatonr ( ' l tuetot'cnt.s Drclis and in natural phytoplanktonpopulations of the Atlantic sector of the Southern Ocean. These findings wcre consistentwith thc role of these carbohydrates upplying energy and carbon skeletons Íbr continuc'rusprote in synthesis .  Addi t ional  ev idcnce lbr  th is  funct ion was provided by ' tC incubut ionexpcrinrents with subsccprent biochemical fractionati<ln clf the incorporated raC int<tseveral pt'xrls, including 'glucan' and 'proteins'. Using a mcldel clcscribing the dynamics inthe glucan pool, it was calculated that the nocturnal respiration rate clf glucan was high,almost two times higher than the diurnirl respiration rate. Thc nocturnal consumption ofglucar.r was found to bc accompanied by continued protein synthesis.The diurnal polysaccharide production decreased with decreasing irradiance, both forC. br<'vis cultures and fbr rratural phyt<lplankton populations. In accordance, Í l .slta thercwas a decrease in the Chl a-normalised polysaccharicle concentration rvith depth. Tlrisdecrease may also lre explaincd by the respiration of pcllysaccharides that were accu-mulated during time spent near the surlàcc. At the Antarctic Polar Front during australautumn 1999, mixing was not deep relative to the depth of the euphotic zone (z.u). Thercserve of carbohydrates was probably onlv important for a patch of phytoplankton thatgot trapped in deeper and dimmcr waters. At the end of the EiscnEx/CARUSO experi-nrent in spring 20(X) nrixing was muclr deeper than 2.,,. In this situation all phytoplanktoncells probably needed a carbclhydrate reserve to continue growth during the timc intervalsthey spcnt at depth while being mixed up and down the watcr column.ró0Hov'does iron limit,The eÍfect of ironexperiment Pcrtorllaboratttry expe rlÍrproduction of watercduced by iron l instorage polysacchametabolism Prc'rvidtThis implics that t lcontent is an indicaThe photochemnotion that Photos)experiments, low ircomplexes in cells cand a lower mirrircluring the ln slnr ir 'felt i l issd patch. Tresponse to the Feacceptor of PSll, QThe nitrogen qobservation is in l i tnitrclgen assimilati<derived reductantrestricted by thc sudiurnal productionC:N diÍ1'ered littlervith the obsewedstressed cells. suggHow is the ffict o1phytoplankton infl'Irr order to studY ttwo ditÏ'erent Photstorage carbohvdrreduced the carbowas co-limited bYlow irradiance warthe photosyntheti,at low irradiancelimited cells whiclincrease in absorlthe package effec'oducÍs irr Artturt tíc;vn ol Antart'tit'l ions: labctratctry cultureoplankton pclpulations, i lt. Thc field cxperimentsn the relative role of ironth in the Southern Ocean.measurement oI storagee most abundant storagerulatc matter was uscd tors polysaccharides. Thee T PTZ ( 2.,{.ír.-r ripyridyl-oducts in Antarcticrg day-night variations inL natural phytoplanktclnfindings were consistentskelutons l i r r  cont inuousrvided by rlC incubation) incorporated laC into:scribing the dynamics inrate of glucan was high,octurnal  consumpt ion o l 'is.sing irradiance, both Íbraccordance, in situ theretration with depth. Thisharides that were accu-rlar Front during austral:uphotic zone (z"u). Thch of phytoplankton thatsenEx/CARUSO experi-ration all phytoplanktonJuring the time intervalsnn.SUIVÍV]ARYHow does iron límítation aJfect the carbohydrate metabolism of Antarctic phytoplankton?The effect of iron l imitation on carbohydrate production was studied in a laboratoryexperiment pcrfbrmed with C. órzr. ' l . i  and during the research expcditions. In thelaboratory expcrimcnts and during the in slla Íèrti l isation experiment. the diurnalpmducticln of water-extractable carbohydrates, the first products of photosynthesis. wasreduced by iron l imitation. ln case thc cclls were nitrogen-limited they would accumulatestorage pcllysaccharides. Therefore, the observcd changes in the storage carbohydratemctabolism provide evidencc that photosynthesis i  the primary target of iron starvation.This implies that the diel change in thc ccllular polysaccharide content, not the averagecontent  is  an in t l icutor  oI  i ron st ress.The photochemical characteristics of iron-stresscd phytoplankton cells supportcd thenotion that photosynthcsis was the primary target of iron l imitation. During the laboratoryexperiments, lclw iron concentrations led to a decrease in the amount of l ight harvestingcirmplexes in cells of C. brevis. This was accompanied by a reduced capacity to absorb l i-ehtand a lclwcr maximal quantum yicld of photochemistry in PSII (Fu:F,,,). In agreement,during the in síttt iron ferti l isation expcriment here was an increasc in F,.:F,,, inside the Fe-ferti l ised patch. The apparent cross scction of photosystem II (oPSII) decreased inresponse to the Fe-rcleasc. as clid the time constant Í irr re-oxidation clf the first quinoneacccptor of PSII, Q,,.The nitrogen quota of C. brevis cells decrcased in response to iron l imitation. Thisobservation is in Iine with those of another research group, who found indications that thenitrogen assimilation of iron-stressed iatoms is l imited by the supply of photosyntheticallyderived rcductant fbr enzymatic rcactions. Alternatively, nitrlgen assimilation may bcrestricted by the supply of carbon skeletons from storage carbohydrates because of the lowdiurnal production of water-extractablc polysaccharides in iron-limitcd cells. The ratio ofC:N diÍïered l itt le between iron-deplete and iron-rcplete C. bravl.s cells. This, combinedwith the observed dccrease in carbohydrate consumption during thc dark period in iron-stresscd cells, suggests that C- and N-metabolism werc sti l l  t ightly couplecl in thcsc cells.How is the elfect of iron limitation on the carbohydrate metaholism of Antarcticphytoplankton influenced by iruadiance?In order to study the combined effects of iron and light l imitation, C. brevis was culturcd attwo difÍèrent photon irradiances, with and without the addition of iron. The production ofstorage carbohydrates was lowcst Íbr cells that werc exposed to low irradiancc. Iron stressreduced thc carbohydrate production even more, which dcmonstrated that the productionwas co-limited by iron and light. A stronger impact of iron on carbohydrate production atlow irradiance was hypothesised, because at this irradiance more iron is required to extendthc photosynthetic apparatus. However. no such interactive effect was evident. Especiallyat low irradiance, there was an incrcase in the Chl a-spccific l ight absorption in iron-limited cells which counteracted the impact of iron stress on photosynthctic eÍficiency. Theincrease in absorption was related to a decrease in cellular pigment content that reducedthe package effect (the self-shading of pigments).r6rSUMMARYAs suggested above, a buffer of storage carbohydrates may allow phytoplankton to maintainhigh growth rates under conditions of deep vertical mixing. Since iron l imitation was foundto reduce the accumulation rate of storage carbohydrates it may affect their function as asource of energy during times spent in deep, dim, waters. It was also observed that iron-stressed C. brevís cells that were cultured at low irradiance, were sensitive to photo-inhibition. This may lead to photodamage in phytoplankton during time spent near theocean surface. The combination of these effects may explain the absence of phytoplanktonblooms (especially of diatoms) in areas with low iron concentrations.Seasonal and regional variations in the role of iron and light in controllíng SouthernOcean phytoplankton growthThe fieldwork presented in this thesis was carried out in the Atlantic sector of the SouthernOcean during austral autumn (1999) and spring (2000), which allows a comparison of therole of iron and light l imitation during these seasons. While phytoplankton responded toiron ferti l isation in spring, there was no response to iron addition during deck incubationsof the resident phytoplankton community in autumn. Indeed, ambient iron concentrationswere somewhat elevated compared to those measured in spring. In autumn, iron-enricheddeep water is transported into the surface layer by entrainment during the deepening of thesurface mixed-layer. The low biomass that was encountered in autumn was likely caused bylight l imitation due to the deep wind mixed layer (>40 m). This was supported by theobservation of a strong reduction in carbohydrate production by phytoplankton duringincubations at an irradiance corresponding to the one at 20-45 min situ depth.During the in situ iron fertilisation experiment in spring, three weeks after the first ironrelease, the areal amount (integral between 0-100 m depth) of water-extractablecarbohydrates had doubled inside the fertilised patch, while remaining roughly constant inthe surrounding waters. Deck incubation experiments revealed that the diurnal chlorophylla-specific production rates of water-extractable polysaccharides were significantly higherfor "in-patch" than for "out-patch" samples. Still, deep mixing induced by several severestorms deteriorated the light climate to such extent that light and iron availability were co-limiting the carbohydrate production. The polysaccharide production was light-limitedwhen cells were incubated at irradiance levels corresponding to those at 20-30 m depth insilu, whereas at certain times the upper mixed layer was several-fold deeper due to storms.Most of the increase in biomass inside the iron-fertilised patch was associated with thefraction of large (>10 pm) phytoplankton cells, consistent with the shift in the communitystructure towards larger diatoms. A stronger response for this fraction was expected, sincelarge cells have a higher halÍ'-saturation constant for iron uptake because of their lowsurface/volume. Still, measurements of diel dynamics in cell size, fluorescence andcarbohydrate amount during the deck-incubation experiments showed that even smallphytoplankton cells responded to iron addition. Yet, there was only a minor increase incell numbers of small species in response to in situ iron fertilisation. It appears likely thattheir biomass was controlled by microzooplankton grazing. The grazing pressure ofmesozooplankton on diatoms does not increase because copepods and other largezooplankton groups have long generation times.During autumncommunity comrelatively high rsurrounding watrsmall species drAntarctic Polarwater, but the ciilphytoplankton bdifference in mirAntarctic Circunm. Possibly, thepressure on smalFinal remarksOne of the overthesis, in whichrelated to chanlinduced by variarhave been perfphytoplankton biin enhanced carafter iron fertilislast long enoughwith this event c(Carbohydrattproduction, sincrthe extracellularthat sink fast.dissolved organiObviously, morea phytoplanktont62,plankton to naintainlimitation was foundct their function as ar observed that iron-: sensitive to photo-time spent near thence of phytoplanktonilling Southernector of the Southerna comparison clf theankton responded toring deck incubationsrt iron concentrationsutumn, iron-enriched, the deepening of ther was likely caused byvas supported by the:hytoplankton duringi depth.:ks after the first ironof water-extractablerg roughly constant inre diurnal chlorophylle significantly higherced by several severen availabil ity were co-ion was light-l imitede at 20-30 m depth lneeper due to storms.s associated with thehift in the communityIn was expected, sincebecause of their lowre, fluorescencc andwed that even smally a minor increase inIt appears l ikely thatgrazing pressure ofrds and other largeSUMIVARYDuring autumn there was a high spatial variation in phytoplankton abundance andcommunity composition. At the Antarctic Polar Front phytoplankton biomass wasrelatively high and the community was dominated by diatoms. In contrast, in thesurrounding waters of the Antarctic Circurnpolar Current biomass was extremely low andsmall species dominated the community. Iron supply may have been higher at theAntarctic Polar Front than in the surrounding waters because of upwelling of iron-richwater, but the differences in iron concentrations were only minor. Likely, the differences inphytoplankton biomass between the front and the waters south of it are related to adifference in mixing depth. The Íiont is a feature with high vertical stability, while in theAntarctic Circumpolar Current beyond the inÍluence of fronts mixing sometimes was > 100m. Possibly, the dominance of diatoms at the front resulted from differential grazingpressure on small phytoplankton cells and diatoms.Final remarksOne of the overarching goals of iron fertilisation experiments is to test the lron Hypo-thesis, in which glacial-interglacial changes in the atmospheric CO2 concentration arerelated to changes in phytoplankton productivity and carbon export to the deep sea,induced by variations in the supply of iron-rich dust. All eight ln sllr iron tèrti l isations thathave lrecn performcd in various ocean regions to date resulted in an increasc inphytoplankton biomass. In spite of all the effort it is not clear whether this increase resultsin enhanced carbon export. In fact, no significant export of carbon has been measuredafter iron Í'ertilisation in any of the experiments. Apart frclm one, the experiments did notlast long enough to capture the final collapse of the bloom scl the carbon export associatedwith this event could not be recorded.Carbohydrate production by phytoplankton may partly determine the exportproduction, since the cellular carbohydrate amount affects the buoyancy of the cells. Also,the extracellular release of carbohydrates plays a role in the formation of large aggregatesthat sink fast. Furthermore. extracellularly released carbohydrates contribute to thedissolved organic carbon pool and may be exported by downwelling of surface water.Obviously, more research is necessary if we want to sketch a full picture of what happens toa phytoplankton population after iron enrichment.163

Iron and light limitation of carbohydrate production by phytoplankton in the Southern Ocean

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Iron and light limitation of carbohydrate production by phytoplankton in the Southern Ocean

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