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 biofilm-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 specific 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
fine-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 float 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
Scientific 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, cofinanced 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
findings 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 final version of
the article.
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