Light Acclimation of the Colonial Green Alga Botryococcus braunii Strain Showa 1[OPEN] Tomas E. van den Berg, a Volha U. Chukhutsina, a,2 Herbert van Amerongen, b Roberta Croce, a,3,4 and Bart van Oort a a Biophysics of Photosynthesis, Department of Physics and Astronomy, Faculty of Sciences, Vrije Universiteit Amsterdam and LaserLaB Amsterdam, 1081 HV Amsterdam, The Netherlands b Laboratory of Biophysics, Wageningen University, 6700 ET Wageningen, The Netherlands ORCID IDs: 0000-0002-7202-4699 (T.E.v.d.B.); 0000-0002-9783-2895 (H.v.A.); 0000-0003-3469-834X (R.C.); 0000-0002-5470-1545 (B.v.O.). In contrast to single cellular species, detailed information is lacking on the processes of photosynthetic acclimation for colonial algae, although these algae are important for biofuel production, ecosystem biodiversity, and wastewater treatment. To investigate differences between single cellular and colonial species, we studied the regulation of photosynthesis and photoprotection during photoacclimation for the colonial green alga Botryococcus braunii and made a comparison with the properties of the single cellular species Chlamydomonas reinhardtii. We show that B. braunii shares some high-light (HL) photoacclimation strategies with C. reinhardtii and other frequently studied green algae: decreased chlorophyll content, increased free carotenoid content, and increased nonphotochemical quenching (NPQ). Additionally, B. braunii has unique HL photoacclimation strategies, related to its colonial form: strong internal shading by an increase of the colony size and the accumulation of extracellular echinenone (a ketocarotenoid). HL colonies are larger and more spatially heterogenous than low-light colonies. Compared with surface cells, cells deeper inside the colony have increased pigmentation and larger photosystem II antenna size. The core of the largest of the HL colonies does not contain living cells. In contrast with C. reinhardtii, but similar to other biolm-forming algae, NPQ capacity is substantial in low light. In HL, NPQ amplitude increases, but kinetics are unchanged. We discuss possible causes of the different acclimation responses of C. reinhardtii and B. braunii. Knowledge of the specic photoacclimation processes for this colonial green alga further extends the view of the diversity of photoacclimation strategies in photosynthetic organisms. Evolutionary differences in microalgae photosyn- thesis are directed by the local light environment. Variations in light intensity and quality combined with the availability of nutrients have shaped a range of ne-tuned algae, adapted to their environmental niches (Croce and van Amerongen, 2014). Within this range of different algae types, many different shapes and sizes are found, from unicells no larger than 1 mm to multi- cellular and colonial species of several centimeters (Beardall et al., 2009). While data on unicellular species provide us with an emerging view on the variations of the photosynthetic apparatus and its regulation, we know little about multicellular and colonial microalgae that have to deal with increased light attenuation (within colonies) and decreased diffusion of nutrients (Beardall et al., 2009). One of these freshwater colonial microalgae is Botryococcus braunii (Trebouxiophycae, Chlorophyta; Weiss et al., 2010), found in lakes and ponds through- out different climate zones (Metzger and Largeau, 2005). This alga has been targeted for biofuel produc- tion since the 1970s because it produces high-quality long-chain hydrocarbons, which are excreted in the extracellular matrix (botryococcenes; Metzger et al., 1985). The oil content of B. braunii colonies can be very high (30%40% of its dry weight; Metzger and Largeau, 2005) and makes the colonies oat close to the water surface, where they can be subjected to high- light (HL) intensities (Wake and Hillen, 1980). Their growth rates are prohibitively low for commercial uti- lization, despite numerous studies aimed at optimizing 1 This work was supported by the Netherlands Organization of Scientic Research (NWO) Earth and Life Sciences (ALW), through a Veni grant to B.v.O. and a Vici grant to R.C., by the NWO-ALW through an MMM grant to R.C., and by a grant from the BioSolar Cell Program, conanced by the Dutch Ministry of Economic Affairs, to R.C. 2 Current address: Department of Life Sciences, Sir Ernst Chain Building, Imperial College London, London SW7 2AZ, UK. 3 Author for contact: r.croce@vu.nl. 4 Senior author. The author responsible for distribution of materials integral to the ndings presented in this article in accordance with the policy de- scribed in the Instructions for Authors (www.plantphysiol.org) is: Roberta Croce (r.croce@vu.nl). R.C. conceived the original research plans; T.E.v.d.B., B.v.O., V.U.C., H.v.A. and R.C. designed the experiments; T.E.v.d.B. per- formed the experiments and analyzed the data; B.v.O. and V.U.C. supervised the experiments and data analysis; T.v.d.B wrote the ar- ticle with contributions of all the authors; R.C. and B.v.O. supervised and completed the writing; all authors approved the nal version of the article. [OPEN] Articles can be viewed without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.18.01499 1132 Plant Physiology Ò , March 2019, Vol. 179, pp. 11321143, www.plantphysiol.org Ó 2019 American Society of Plant Biologists. All Rights Reserved. www.plantphysiol.org on May 24, 2020 - Published by Downloaded from Copyright © 2019 American Society of Plant Biologists. All rights reserved.