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Influence of Nutrients and Light on Autotrophic, Mixotrophic and Heterotrophic Freshwater Chrysophytes

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Influence of Nutrients and Light on Autotrophic, Mixotrophic and Heterotrophic Freshwater Chrysophytes Vol. 71: 179–191, 2013 AQUATIC MICROBIAL ECOLOGY Published online December 16 doi: 10.3354/ame01662 Aquat Microb Ecol Influence of nutrients and light on autotrophic, mixotrophic and heterotrophic freshwater chrysophytes Julia Rottberger1,*, Ansgar Gruber1, Jens Boenigk2, Peter G. Kroth1 1Plant Ecophysiology, Department of Biology, Universität Konstanz, 78457 Konstanz, Germany 2Department of Botany, Universität Duisburg-Essen, 45117 Essen, Germany ABSTRACT: Chrysophyte algae show wide variation in their nutritional modes, which can be espe- cially advantageous in oligotrophic conditions. However, the capacities and strategies of the algae to adapt to changing conditions may vary due to different nutritional requirements of individual species. In this context, comparative analyses evaluating the physiological range of mixotrophic chrysophytes are important to predict possible changes in phytoplankton composition. We com- pared 4 freshwater chrysophytes — Poteriospumella lacustris, Poterioochromonas malhamensis, Di- nobryon divergens and Mallomonas annulata — under different growth conditions. The diatom Phaeodactylum tricornutum served as a photoautotrophic reference strain. We demonstrate active growth of P. lacustris and the mixotrophic P. malhamensis under chemoheterotrophic conditions. Neither of the chrysophytes were growing photoautotrophically; however, P. malhamensis showed some photosynthetic activity and survived longer when kept in the light. M. annulata, P. tricor - nutum and the mixotrophic D. divergens showed light-limited growth when kept in inorganic me- dia. Even though D. divergens consumed living bacteria, it did not grow in the dark in the presence of the bacteria only. We detected large differences in the general nutritional preferences between the 2 mixotrophs in relation to the nutritional features of all investigated strains. KEY WORDS: Mixotrophy · Oxygen evolution · Carbon · Culturing conditions · Phaeodactylum tricornutum Resale or republication not permitted without written consent of the publisher INTRODUCTION and because they often dominate mixotrophic phyto- plankton populations (De Hoyos et al. 1998, Watson et Mixotrophic algae are able to meet their carbon de- al. 2001, Kamjunke et al. 2007). Chrysophytes are geo - mands by assimilating inorganic carbon (CO2) as well graphically widespread and abundant in freshwater as by taking up organic molecules. The uptake of or- and marine habitats as well as in soils (Sandgren ganic substances is not limited to dissolved molecules 1988, Boenigk & Arndt 2002, Massana 2011). While a (osmotrophy) but can also be accomplished by inges- large number of chrysophyte genera show mixotro- tion of detritus or living bacteria (phagotrophy). phic traits (Porter 1988, Sanders & Porter 1988), all the Chrysophytes (throughout the manuscript, this term different metabolic lifestyles ranging from exclusively refers to the chrysophytes sensu lato, comprising the chemoheterotrophic to exclusively photoautotrophic classes Chrysophyceae and Synurophyceae [Ander- nutrition can be found (Raven et al. 1995). sen et al. 1999, Kristiansen & Preisig 2007, Jordan & Several parameters may affect the growth compet- Iwataki 2012]) are of special interest because their itiveness of mixotrophic chrysophytes. Besides car- abundance may increase during phases of lake re- bon and phosphorous availability (Rothhaupt 1996a), oligotrophication (Gaedke 1998, Jeppesen et al. 2005) light (de Castro et al. 2009), pH (Moser & Weisse *Email: [email protected] © Inter-Research 2013 · www.int-res.com 180 Aquat Microb Ecol 71: 179–191, 2013 2011b) and temperature (Moser & Weisse 2011a, NiCl2 and with addition of dissolved organic matter Wilken et al. 2013) have also been shown to be (DOM) sources of 1 g l−1 peptone (Roth), 1 g l−1 yeast important factors in laboratory studies. Furthermore, extract (Roth) and 1 g l−1 α-D-glucose. Dinobryon some chrysophytes require vitamin supply (Heinrich divergens and Mallomonas annulata were grown 1955). Mixotrophic chrysophytes are thought to be in liquid WC medium (pH 8) (Guillard & Lorenzen very competitive in oligotrophic waters because 1972) with modified concentrations of TES buffer some of them may ingest bacteria, which are utilized (C6H15NO6S 500 µM), NaHCO3 (375 µM), K2HPO4 as carbon and phosphorus source (Thingstad et al. (32 µM), NaNO3 (500 µM) and MnCl2 (0.09 µM). The 1996, Kamjunke et al. 2007, Unrein et al. 2007). Still, standard medium for Poterioochromonas malhamen- each of the mentioned parameters is likely to affect sis was modified bacillariophycean medium (BM) (pH each chrysophyte species in a different way (Watson 7.2) (Schlösser 1994) with 236 µM Na2CO3, 27 µM & McCauley 2010, Moser & Weisse 2011b), making it iron(III) citrate hydrate, 214 µM citric acid, 60 nM −1 −1 difficult to predict the success of certain mixotrophic MnSO4, 200 µg l thiamine-HCl, 10 µg l biotin and species under changing conditions. DOM. Phaeodactylum tricornutum was grown in In the present study, we compare nutritionally dif- modified f/2 medium (pH 7) (Guillard & Ryther 1962, ferent mixotrophic chrysophyte species to each other Guillard 1975) with artificial half-concentrated sea salts as well as to purely photoautotrophic or purely (16.6 g l−1 Tropic Marin®, Dr. Biener) and 0.09 µM chemoheterotrophic reference species. We aimed to manganese or on solid plates of modified f/2 (with demonstrate how different chrysophytes are affected 1.5% agar) for culture maintenance. The axenic state by nutritional parameters under identical conditions of the cultures was monitored regularly by light and and by this to understand whether the observed dif- fluorescence microscopy, using an automatic particle ferences may influence the competitive fitness of a counter and by screening culture aliquots for growth single species. To this end, we tested different cultur- of bacterial colonies on solid media (1.5% agar) con- ing conditions in order to find the most suitable condi- taining DOM. A consortium of several bacterial tions for physiological comparisons. Further, we spec- strains served as prey during feeding experiments. ified which component of the culturing media limited The bacteria were isolated from Dinobryon divergens maximum cell numbers of each protist to make sure cultures by plating a culture sample on WC medium that the macronutrients and not the trace metals or vi- including DOM and incubating the plate for 1 wk at tamins were the limiting factor. We performed com- room temperature. The bacterial consortium was parative studies examining the influence of light and transferred to fresh plates monthly without further different carbon sources on all strains. Additionally, purification. The bacteria were grown in liquid WC we compared photosynthetic capacities of all strains medium with DOM for feeding experiments. by conducting oxygen evolution measurements to Cultures were generally grown at 20°C in Erlen- complement results from the growth experiments. meyer flasks without shaking under sterile condi- tions and at a light intensity of 30 to 40 µmol photons m−2 s−1 on the surface of the culture flasks. If not MATERIALS AND METHODS noted otherwise, the light:dark cycle was 16 h:8 h. Strains and standard culturing conditions Cell counts of protists The chrysophytes investigated in the present study were isolated from oligotrophic, alpine or pre-alpine Cell counts and the determination of the biovolume freshwaters (Table 1) and include 2 mixotrophic of protists were performed with an automatic particle strains, Dinobryon divergens FU18K_A (xenic) and counter according to the Coulter principle (‘Coulter Poterioochromonas malhamensis DS (axenic). The counter’, Multisizer III, Beckman Coulter) using a colourless heterotrophic Poteriospumella lacustris capillary with an aperture of 100 µm diameter. (strain JBM10) (axenic) and the photoautotrophic Directly prior to measurements, 100 to 900 µl of a cell Mallomonas annulata WA 18K_M (xenic) were cho- suspension were diluted in 12 ml of the electrolyte sen as reference strains. As a photoautotrophic refer- IsotonII-Diluent (Beckman Coulter) by pipetting. ence strain, we also studied the diatom Phaeodacty- Measurements were performed in triplicates for each lum tricornutum UTEX646. sample and averaged. To reduce background signals Poteriospumella lacustris was cultured in modified from dust, precipitates and fibers, a sample of the inorganic basal medium (pH 7.2) (Hahn 2003) without sterile control was analyzed and subtracted. To gain Rottberger et al.: Physiology of chrysophytes 181 Table 1. Algal strains investigated in the present study Algal strain and origin Axenic ? Reference for Carbon Habitus References for strain description acquisition phagotrophy Mallomonas annulata WA 18K_M Lake Wallersee, Austria No J. Boenigk (unpubl.) Autotroph Unicellular None Dinobryon divergens FU 18K-A Lake Fuschelsee, Austria No J. Boenigk (unpubl.) Mixotroph Colonial Jones & Rees (1994), Veen (1991) Poterioochromonas malhamensis DS Lake Constance, Germany Yes Hahn & Höfle (1998) Mixotroph Unicellular, Hahn & Höfle (1998) stalks Poteriospumella lacustris JBM10 Lake Mondsee, Austria Yes Findenig et al. (2010) Heterotroph Unicellular Boenigk et al. (2006) Phaeodactylum tricornutum Bohlin UTEX 646 Baltic Sea, Finland No Droop (1954), Autotroph Unicellular None De Martino et al. (2007) the cell density (i.e. cell number per milliliter), the related to microscopic cell counts of living bacteria curve area corresponding to the algal
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