Abstract
Marine phytoplankton, and in particular diatoms, are responsible for almost half of all primary production on Earth. Diatom species thrive from polar to tropical waters and across light environments that are highly complex to relatively benign, and so have evolved highly divergent strategies for regulating light capture and utilization. It is increasingly well established that diatoms have achieved such successful ecosystem dominance by regulating excitation energy available for generating photosynthetic energy via highly flexible light harvesting strategies. However, how different light harvesting strategies and downstream pathways for oxygen production and consumption interact to balance excitation pressure remains unknown. We therefore examined the responses of three diatom taxa adapted to inherently different light climates (estuarine Thalassioisira weissflogii, coastal Thalassiosira pseudonana and oceanic Thalassiosira oceanica) during transient shifts from a moderate to high growth irradiance (85 to 1200 μmol photons m-2 s-1). Transient high light exposure caused T. weissflogii to rapidly downregulate PSII with substantial nonphotochemical quenching, protecting PSII from inactivation or damage, and obviating the need for induction of O2 consuming (light-dependent respiration, LDR) pathways. In contrast, T. oceanica retained high excitation pressure on PSII, but with little change in RCII photochemical turnover, thereby requiring moderate repair activity and greater reliance on LDR. T. pseudonana exhibited an intermediate response compared to the other two diatom species, exhibiting some downregulation and inactivation of PSII, but high repair of PSII and induction of reversible PSII nonphotochemical quenching, with some LDR. Together, these data demonstrate a range of strategies for balancing light harvesting and utilization across diatom species, which reflect their adaptation to sustain photosynthesis under environments with inherently different light regimes.
Highlights
Diatoms account for the majority of marine primary production [1, 2] and are ubiquitous across aquatic environments [3], from tropical to polar regions, and from highly dynamic coastal and upwelling habitats to more stable oceanic waters
Excitation allocation strategies were investigated in diatoms species with different ecological niches; the coastal pennate Phaeodactylum tricornutum, coastal small centric Chaetoceros muelleri, coastal large centric Ditylum brightwellii, and four centric species of the Thalassiosira genus ranging in cell size from smallest to largest: coastal T. pseudonana, open ocean T. oceanica, esturaine T. weissflogii, coastal T. rotula
Overall, increased reliance on non-photochemical quenching generally corresponded with decreased photochemical quenching, tracking the remaining fraction of RCIIs engaged in photochemistry, across these three species
Summary
Diatoms account for the majority of marine primary production [1, 2] and are ubiquitous across aquatic environments [3], from tropical to polar regions, and from highly dynamic coastal and upwelling habitats to more stable oceanic waters. Failure to regulate excess excitation energy either as photons reaching the reaction centre or as harvested energy (i.e. electrons) within the electron transport chain can increase the probability of photoinactivation of photosystem II (PSII, [13]), likely from the generation of reactive oxygen species [14], leading to a decrease in net primary productivity and growth. One of the most important mechanisms for rapid (on the order of seconds to minutes) regulation of photochemistry under high light is non-photochemical quenching (see [15] review), parameterized as a yield, YNPQ (equivalent to FNPQ [16] and conceptually similar to [1-Q] [17]), whereby excitation energy in excess of the photosynthetic capacity, is safely dissipated as heat by light harvesting pigment complexes associated with PSII (LHCII, [18, 19]). YNO comprises constitutive thermal losses [16] as well as intrinsic losses (sensu [20])
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