Short- and long-term acclimation patterns of the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) along a depth gradient.

The giant kelp, Macrocystis pyrifera, is exposed to highly variable irradiance and temperature regimes across its geographic and vertical depth gradients. The objective of this study was to extend our understanding of algal acclimation strategies on different temporal scales to those varying abiotic conditions at various water depths. Different acclimation strategies to various water depths (0.2 and 4 m) between different sampling times (Jan/Feb and Aug/Sept 2012; long-term acclimation) and more rapid adjustments to different depths (0.2, 2 and 4 m; short-term acclimation) during 14 d of transplantation were found. Adjustments of variable Chl a fluorescence, pigment composition (Chl c, fucoxanthin), and the de-epoxidation state of the xanthophyll cycle pigments were responsible for the development of different physiological states with respect to various solar radiation and temperature climates. Interestingly, the results indicated that phlorotannins are important during long-term acclimation while antioxidants have a crucial role during short-term acclimation. Furthermore, the results suggested that modifications in total lipids and fatty acid compositions apparently also might play a role in depth acclimation. In Aug/Sept (austral winter), M. pyrifera responded to the transplantation from 4 m to 0.2 m depth with a rise in the degree of saturation and a switch from shorter- to longer-chain fatty acids. These changes seem to be essential for the readjustment of thylakoid membranes and might, thus, facilitate efficient photosynthesis under changing irradiances and temperatures. Further experiments are needed to disentangle the relative contribution of solar radiation, temperature and also other abiotic parameters in the observed physiological changes.

Transcriptomic analysis of metabolic function in the giant kelp, Macrocystis pyrifera, across depth and season.

To increase knowledge of transcript diversity for the giant kelp, Macrocystis pyrifera, and assess gene expression across naturally occurring depth gradients in light, temperature and nutrients, we sequenced four cDNA libraries created from blades collected at the sea surface and at 18 m depth during the winter and summer. Comparative genomics cluster analyses revealed novel gene families (clusters) in existing brown alga expressed sequence tag data compared with other related algal groups, a pattern also seen with the addition of M. pyrifera sequences. Assembly of 228 Mbp of sequence generated c. 9000 isotigs and c. 12,000 open reading frames. Annotations were assigned using families of hidden Markov models for c. 11% of open reading frames; M. pyrifera had highest similarity to other members of the Phaeophyceae, namely Ectocarpus siliculosus and Laminaria digitata. Quantitative polymerase chain reaction of transcript targets verified depth-related differences in gene expression; stress response and light-harvesting transcripts, especially members of the LI818 (also known as LHCSR) family, showed high expression in the surface compared with 18 m depth, while some nitrogen acquisition transcripts (e.g. nitrite reductase) were upregulated at depth compared with the surface, supporting a conceptual biological model of depth-dependent physiology.

Addition of species abundance and performance predicts community primary production of macroalgae.

Understory plant assemblages are important sources of primary production in both terrestrial and marine environments, and they may exhibit different dynamics than their overstory counterparts. For example, production within dense upper canopies is typically light-limited by shading, whereas such canopy architecture effects are likely unimportant in low-light environments, such as those inhabited by sparser understory assemblages. In these assemblages, light saturation of understory production may be common as species become limited by their photosynthetic capacity, which is adapted to low-light levels. Here we show that a simple model relating species-specific light use relationships measured in the laboratory to biomass and light levels measured in nature accurately predicts community gross primary production (GPP) in a marine understory algal community. We validate the model by comparing GPP measured in situ in enclosed chambers with model estimates for the same incubations. Model estimates of GPP explained 70% of the variation in the measured estimates. The results show that GPP was accurately estimated by simple addition of the photosynthetic capacity of each species in the community based on their biomass and the available light. The difference between modeled and measured GPP did not show any relationship with community biomass or diversity, and the results suggest that diversity does not significantly affect productivity in this system. This type of model should be applicable in other environments where canopy architecture does not play a significant role in limiting photosynthesis.

Photoprotection in the brown alga Macrocystis pyrifera: evolutionary implications.

The dissipation of energy as heat is essential for photosynthetic organisms to protect themselves against excess light. We compared Photosystem II florescence changes (non-photochemical quenching, NPQ) in the brown alga Macrocystis pyrifera with that of Ficus sp., a higher plant to examine if the mechanism of heat dissipation (energy-dependent quenching, qE) differs between these evolutionary distant groups of phototrophs. We discovered that M. pyrifera had a slower rise of NPQ upon illumination than the Ficus sp. Further, the NPQ relaxation phase that takes place in the first minutes after light to dark transition is absent in this brown alga. We found that the NPQ induction rate in this alga was 1.5 times faster in preilluminated samples than in dark-adapted samples; this was associated with an increase in the rate of accumulation of the carotenoid zeaxanthin. Therefore, we conclude that NPQ in M. pyrifera is associated only with the formation of zeaxanthin. These results indicate that M. pyrifera lacks the fast component of qE that is related to allosteric changes in the light harvesting complexes of Ficus sp., a representative of higher plants. Although the xanthophyll cycle of this brown alga is similar to that of Ficus sp., yet, the transthylakoid proton gradient (ΔpH) does not influence NPQ beyond the activation of the violaxanthin de-epoxidase enzyme. These findings suggest that NPQ control mechanisms are not universal and we suggest that it may have diverged early in the evolution of different groups of eukaryotic phototrophs.

The giant kelp Macrocystis pyrifera presents a different nonphotochemical quenching control than higher plants.

Here the mechanisms involved in excitation energy dissipation of Macrocystis pyrifera were characterized to explain the high nonphotochemical quenching of chlorophyll a (Chla) fluorescence (NPQ) capacity of this alga. We performed a comparative analysis of NPQ and xanthophyll cycle (XC) activity in blades collected at different depths. The responses of the blades to dithiothreitol (DTT) and to the uncoupler NH4Cl were also assayed. The degree of NPQ induction was related to the amount of zeaxanthin synthesized in high light. The inhibition of zeaxanthin synthesis with DTT blocked NPQ induction. A slow NPQ relaxation upon the addition of NH4Cl, which disrupts the transthylakoid proton gradient, was detected. The slow NPQ relaxation took place only in the presence of de-epoxidated XC pigments and was related to the epoxidation of zeaxanthin. These results indicate that in M. pyrifera, in contrast to higher plants, the transthylakoid proton gradient alone does not induce NPQ. The role of this gradient seems to be related only to the activation of the violaxanthin de-epoxidase enzyme.