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Sizespectrum Based Differential Response of Phytoplankton To bs_bs_banner Phycological Research 2014 Size-spectrum based differential response of phytoplankton to nutrient and iron-organic matter combinations in microcosm experiments in a Chilean Patagonian Fjord Jose L. Iriarte,1,2* Murat V. Ardelan,3 Luis Antonio Cuevas,4 Humberto E. González,5,2 Nicolas Sanchez3 and Sverne M. Myklestad6 1Instituto de Acuicultura and Centro de Investigación en Ecosistemas de la Patagonia-CIEP, Universidad Austral de Chile, Puerto Montt, 2COPAS Sur-Austral, 4Centro de Ciencias Ambientales EULA-Chile, Universidad de Concepción, Concepción, 5Instituto de Ciencias Marinas y Limnológicas and Centro de Investigación en Ecosistemas de la Patagonia-CIEP, Universidad Austral de Chile, Valdivia, Chile, Departments of 3Chemistry and 6Biotechnology, NTNU, Norwegian University of Science and Technology, Trondheim, Norway teria through the interaction with organic ligands SUMMARY released by bacteria that eventually could increase solubility of the Fe dissolved fraction thus having The Patagonian fjords have been recognized as a major a positive effect on the small-sized phytoplankton region of relatively high primary productivity systems community. during spring–summer bloom periods, where iron- organic matter forms may be essential complexes Key words: Iron-dissolved organic matter, micro- involved in key growth processes connected to the phytoplankton, Patagonia fjord, polysaccharide, carbon and nitrogen cycles. We used two dissolved siderophore, Synechococcus. organic matter (DOM) types, marine polysaccharide and siderophore, as a model to understand how they affect the bioavailability of Fe to phytoplankton and bacteria and to assess their ecological role in fjord systems. A 10-day microcosm study was performed in INTRODUCTION the Comau Fjord during summer conditions (March Iron as a micronutrient is an essential enzymatic 2012). Pico-, nano-, and microphytoplankton abun- co-factor for photosynthesis, respiration, and macronu- dance, total chlorophyll-a and bacteria abundance, trient assimilation (Morel & Price 2003), nevertheless and bacterial secondary production estimates were micronutrient requirements can differ among phyto- analyzed in five treatments: (i) control (no additions), plankton taxa (Yang & Jiao 2002; Tsuda et al. 2005) (ii) only nutrients (NUT: PO4,NO3, Si), (iii) nutri- as did their impact as a limiting factor. In temperate + ents Fe(II), (iv) polysaccharide (natural diatoms coastal regions, in addition to the typical spring– extracted: 1–3 beta Glucan), and (v) Hexandentate summer conditions such as high solar radiation and Desferroxiamine B (DFB, siderophore). Our results macronutrients availability, we should also consider showed that while DFB reduced Fe bioavailability for the release of Fe from strong riverine sources as almost all phytoplankton assemblages in the fjord, another element that may influence the seasonal polysaccharide did not have effects on the iron cycle and magnitude of primary productivity (PP) and + bioavailability. At Nutrients Fe and Polysaccharide phytoplankton growth. Due to terrestrial (riverine), treatments, chlorophyll-a concentration abruptly aeolian dust, and water column-sediment sources of −3 increased from 0.9 to 20 mg m during the first 4–6 micronutrients and dissolved organic matter (DOM), days of the experimental period. Remarkably, at the the distribution, speciation, and transformation of dif- + Nutrients Fe treatment, the development of the ferent forms of micronutrients are more dynamic and bloom was accompanied by markedly high abundances complex in near-shore water than in oceanic water. In of Synechococcus, picoeukaryotes, and autotrophic nanoflagellates within the first 4 days of the experi- ment. Our study indicated that small plankton (phyto- < μ plankton 20 m and bacteria) were the first to *To whom correspondence should be addressed. + respond to dissolved Nutrients Fe compared to large Email: [email protected] sized micro-phytoplankton cells (>20 μm). This could Communicating editor: J. H. Kim. be at least partially attributed to biological utilization Received 6 April 2013; accepted 1 December 2013. of Fe (2 to 3 nM) by <20 μm phytoplankton and bac- doi: 10.1111/pre.12050 © 2014 Japanese Society of Phycology 2 J. L. Iriarte et al. spite of that, the importance of DOM as a significant Preliminary observations indicated that concentra- micronutrient ‘carrier’ for PP in coastal areas with tions of Fe in Comau Fjord are relatively low (2–3 nM, freshwater influence has not been fully elucidated. Ardelan et al. 2009b), compared to concentrations in Various DOM may have important effects on iron spe- those in other coastal areas (Bruland et al. 2001; ciation and hence its bioavailability to phytoplankton Öztürk & Bizsel 2002), suggesting a critical role in assemblages. Some DOM may convert available Fe the dynamics of phytoplankton in Patagonian fjords. form into not fully bioavailable Fe form (Öztürk & However, micronutrient availability, and in turn Bizsel 2002; Öztürk et al. 2002), thus it could be the primary productivity rate, can be affected by critical in marine areas where dissolved Fe (DFe) con- complexation with organic matter and colloids forma- centrations are already low. Furthermore, the additions tions (Öztürk et al. 2002). Terrestrial-derived organic of macronutrients to the system relative to Fe may also matter (e.g. humic acids), as well as biologically contribute to controlling the role of Fe on phytoplank- released agents (e.g. bacterial siderophores), are impor- ton structure and function. From the chemical point of tant DOM sources in aquatic systems. It has been view, both dissolved and particulate organic matter suggested that the complexation of micronutrients with (DOM and POM), as well as the lithogenic and DOM may reduce the availability of micronutrient biogenic fractions of the POM, constituted very elements, thus limiting the PP in aquatic systems complex pools with a high heterogeneity degree in sub- (Wells & Trick 2004). In iron-replete coastal waters it stance classes responsible for metal binding (Boyd has been observed that increasing concentrations of et al. 2010; Strmecki et al. 2010), usually loaded siderophores decreased the biological availability of with a highly variable amount of microelements such iron added to natural seawater (Wells & Trick 2004). as Fe. Thus, the growth response of phytoplankton Furthermore, the presence of hydroxycarboxylic acid exposed to different concentrations of natural DOM (e.g. glucaric acid) positively influenced iron availability would be difficult to analyse. A simple design to tackle to phytoplankton assemblages in the Southern Ocean this relevant problem is to assay single DOM com- (Öztürk et al. 2004). Marine polysaccharide and pounds and their capacity to form chelate complexes siderophore complexing capacities with Fe following with limiting micronutrients (i.e., DOM ligands +Fe) the growth of natural phytoplankton assemblages is still required for phytoplankton and bacterial growth. an open question (Hassler et al. 2011). We postulated Although current studies favor Fe availability as the that different phytoplankton species and/or functional main factor limiting PP in high nutrient low chlorophyll groups have different biological capacities to utilize (HNLC) oceanic regions (Bruland et al. 2001), biologi- these Fe-DOM complexes. Fe-DOM formation exerted cal availability of Fe–DOM interactions affecting cellular by heterotrophic bacteria in natural waters was also uptake processes of Fe on phytoplankton growth in addressed in this study, and the heterotrophic bacteria coastal areas require more attention. Specifically, the abundance and bacterial secondary production was growth and species composition of phytoplankton monitored to follow the bacterial evolution in our treat- assemblages in the ocean HNLC regions are often regu- ments in relationship with phytoplankton growth. The lated by iron (Tsuda et al. 2005), which in turn influ- main objective of this study was to determine the ences oceanic PP.From modeling results, the chemically effects of two different DOM on Fe bioavailability for important role of DOM in controlling free micronutrients pico-, nano-, and microphytoplankton abundance, in seawater (Hirose 2007), and their uptake by phyto- total autotrophic biomass, and species composition of plankton, is known. Due to seasonal climatologic- microphytopankton in Comau Fjord, Patagonia. For this oceanographic features in coastal temperate areas, purpose, an in situ experimental microcosm setting was temporal growth limitation by Fe can also be expected performed by using two different types of DOM to (Bruland et al. 2001; Hutchins et al. 2002; Öztürk et al. manipulate Fe bioavailability at the Comau Fjord during 2002; Torres & Ampuero 2009). Since Patagonian fjords austral summer. Knowledge is still scarce on phyto- have been suggested as major ‘CO2 sink’ areas, under- plankton capacity for biological uptake and macronu- standing the processes/factors that modulate the effi- trient metabolism (such as nitrate and ammonia), ciency of the biological pump in this ecosystem will be linked to the bioavailability of Fe, forming complexes in relevant. Early results strongly suggest that nitrogen a nutrient modified scenario in the Patagonia fjords source (mainly inorganic such as nitrate and ammonia) system where aquaculture may act as an important inputs could play a major role in sustaining relatively source of new nitrogen and DOM. Specifically, increas- large PP (mean
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