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Pigment Composition and Photoacclimation As Keys to the Ecological Success of Gonyostomum Semen (Raphidophyceae, Stramenopiles)

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Pigment Composition and Photoacclimation As Keys to the Ecological Success of Gonyostomum Semen (Raphidophyceae, Stramenopiles) Pigment composition and photoacclimation as keys to the ecological success of Gonyostomum semen (Raphidophyceae, Stramenopiles) Sassenhagen, Ingrid; Rengefors, Karin; Richardson, Tammi L.; Pinckney, James L. Published in: Journal of Phycology DOI: 10.1111/jpy.12246 2014 Link to publication Citation for published version (APA): Sassenhagen, I., Rengefors, K., Richardson, T. L., & Pinckney, J. L. (2014). Pigment composition and photoacclimation as keys to the ecological success of Gonyostomum semen (Raphidophyceae, Stramenopiles). Journal of Phycology, 50(6), 1146-1154. https://doi.org/10.1111/jpy.12246 Total number of authors: 4 General rights Unless other specific re-use rights are stated the following general rights apply: Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal Read more about Creative commons licenses: https://creativecommons.org/licenses/ Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. LUND UNIVERSITY PO Box 117 221 00 Lund +46 46-222 00 00 J. Phycol. 50, 1146–1154 (2014) © 2014 The Authors. Journal of Phycology published by Wiley Periodicals, Inc. on behalf of Phycological Society of America. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. DOI: 10.1111/jpy.12246 PIGMENT COMPOSITION AND PHOTOACCLIMATION AS KEYS TO THE ECOLOGICAL SUCCESS OF GONYOSTOMUM SEMEN (RAPHIDOPHYCEAE, STRAMENOPILES)1 Ingrid Sassenhagen,2 Karin Rengefors Aquatic Ecology, Department of Biology, Lund University, Solvegatan€ 37, Lund 22362, Sweden Tammi L. Richardson, and James L. Pinckney Department of Biological Science, University of South Carolina, 712 Sumter Street, Columbia, South Carolina 29208, USA Aquatic habitats are usually structured by light matter; HPLC, high performance liquid chromatog- attenuation with depth resulting in different raphy; neox, neoxanthin; violax, violaxanthin; zeax, microalgal communities, each one adapted to a zeaxanthin certain light regime by their specific pigment composition. Several taxa contain pigments restricted to one phylogenetic group, making them useful as Microalgae are usually highly adapted to different marker pigments in phytoplankton community light conditions, populating habitats suited for their studies. The nuisance and invasive freshwater specific pigment composition and absorption max- microalga Gonyostomum semen (Raphidophyceae) is ima. This is especially evident in marine ecosystems, mainly found in brown water lakes with sharp vertical as stratified water columns and significant changes gradients in light intensity and color. However, its in light intensity and color often cause selection pigment composition and potential photoadaptations and niche partitioning of phytoplankton taxa have not been comprehensively studied. We analyzed according to the prevailing light environment the photopigment composition of 12 genetically (Bidigare et al. 1990a, Stomp et al. 2004, Hickman different strains of G. semen by high performance et al. 2009). For example, Bidigare et al. (1990a) liquid chromatography after acclimation to different observed a vertically structured distribution of differ- light conditions. We confirmed the pigments chl a, ent phytoplankton taxa (cyanobacteria, diatoms, chl c1c2, diadinoxanthin, trans-neoxanthin, cis- and prymnesiophytes) in the Sargasso Sea suggesting neoxanthin, a and b carotene, which have already chromatic adaptation. Picoplanktonic cyanobacteria been reported for G. semen. In addition, we like Synechococcus sp. and Prochlorococcus sp. are well- identified, for the first time, the pigments violaxan- adapted to high irradiance in blue tropical waters thin, zeaxanthin, and alloxanthin in this species. by generating high concentrations of the photopro- Alloxanthin has never been observed in tective pigment zeaxanthin (zeax) (Lutz et al. 2003, raphidophytes before, suggesting differences in Hickman et al. 2009). evolutionary plastid acquisition between freshwater In environments with varying light conditions, lineages and the well-described marine species. The photoacclimation is frequently manifested as altera- amount of total chl a per cell generally decreased tions in the photosynthetic pigment content in with increasing light intensity. In contrast, the response to changing irradiance (MacIntyre et al. increasing ratios of the prominent pigments 2002). Haptophytes, for example, adjust to heteroge- diadinoxanthin and alloxanthin per chl a with light neous light climates through highly plastic concentra- intensity suggest photoprotective functions. In tions of fucoxanthin-related carotenoids. The addition, we found significant variation in cell- concentrations of these pigments per chl a can differ specific pigment concentration among strains, among haptophyte species and strains (Buma et al. grouped by lake of origin, which might correspond to 1991, Stolte et al. 2000). Thus, acclimation does not genetic differences between strains and populations. involve a change in the genetic structure of the popu- Key index words: Gonyostomum semen lation under investigation whereas adaptation does. alloxanthin; ; The nuisance freshwater microalga Gonyostomum HPLC; photoacclimation; pigments; raphidophyte semen (Ehrenberg) has recently spread to several new Abbreviations: allo, alloxanthin; chl, chlorophyll; habitats and currently dominates the phytoplankton diadino, diadinoxanthin; DOM, dissolved organic community in many Scandinavian lakes (Lepisto€ et al. 1994, Rengefors et al. 2012, Lebret et al. 2013). 1Received 10 March 2014. Accepted 21 July 2014. Originally, it was encountered in dark, brown water 2Author for correspondence: e-mail [email protected]. lakes (Sorensen€ 1954) with very sharp gradients of Editorial Responsibility: L. Graham (Associate Editor) 1146 PIGMENT COMPOSITION AND PHOTOACCLIMATION IN GONYOSTOMUM 1147 light intensity because of rapid attenuation of light species at six different light intensities to study with depth. In these lakes, it may form extensive intra-specific differences and changes in pigment blooms during the summer and its cell number can concentration because of photoacclimation. We represent up to 97% of the phytoplankton commu- hypothesized that G. semen is equipped with a very nity (Cronberg et al. 1988, Findlay et al. 2005, Lebret powerful light harvesting system to effectively photo- et al. 2012b). Gonyostomum semen is considered a nui- synthesize under low light intensity, but negligible sance species, as its mucous threads and trichocysts photoprotective capabilities since they can migrate may cause skin irritation in swimmers (Sorensen€ downwards to avoid supersaturating irradiance. As 1954). Its rapid expansion and high competitiveness the strains originated from habitats with different has recently aroused much scientific interest. There water color and light conditions, we expected to is evidence that a lack of grazers, the ability to feed find significant differences in pigment ratios among heterotrophically on dissolved organic matter strains because of genetic adaptation to local (DOM), preferences for low pH and higher water environmental conditions. temperatures enable this species to outcompete other algae (Findlay et al. 2005, Rengefors et al. 2008, Le- bret et al. 2012a, Rengefors et al. 2012, Johansson MATERIALS AND METHODS et al. 2013). Furthermore, G. semen is able to migrate Culturing conditions and microscopy. Twelve genetically dis- vertically through the water column (Cronberg et al. tinct strains of the microalgae G. semen, which were distin- 1988, Salonen and Rosenberg 2000), presumably as a guished earlier by amplified fragment length polymorphism way of choosing an optimal light intensity for photo- (Lebret et al. 2013), were used for this experiment. These synthesis during the day, and at night it migrates strains originated from five lakes with varying absorbance down in anoxic zones below the thermocline to (Table 1), resulting in different light climates. Cultures were incubated for 6 weeks at six different light conditions (5, 10, access higher nutrient concentrations (Salonen and À2 À1 25, 150, 200 lmol photons Á m Á s of white light and À À Rosenberg 2000). This is an important advantage in 25 lmol photons Á m 2 Á s 1 of red light, AURA Luminette the competition with many other microalgae, which 36W 840, Aura Light International AB, Karlskrona, Sweden) are dependent on buoyancy or suspension for access in artificial medium (modified Woods Hole medium, pH 7.0; to light near to the surface (Olli 1999, Richardson Guillard and Lorenzen 1972). The red light climate was et al. 2001). Despite the importance of light as a achieved by filtering out all other wavelength (<600 nm) with structuring environmental
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