Red-light phenotype in a marine diatom involves a specialized oligomeric red-shifted antenna and altered cell morphology

Abstract

Diatoms greatly contribute to carbon fixation and thus strongly influence the global biogeochemical balance. Capable of chromatic acclimation (CA) to unfavourable light conditions, diatoms often dominate benthic ecosystems in addition to their planktonic lifestyle. Although CA has been studied at the molecular level, our understanding of this phenomenon remains incomplete. Here we provide new data to better explain the acclimation-associated changes under red-enhanced ambient light (RL) in diatom Phaeodactylum tricornutum, known to express a red-shifted antenna complex (F710). The complex was found to be an oligomer of a single polypeptide, Lhcf15. The steady-state spectroscopic properties of the oligomer were also studied. The oligomeric assembly of the Lhcf15 subunits is required for the complex to exhibit a red-shifted absorption. The presence of the red antenna in RL culture coincides with the development of a rounded phenotype of the diatom cell. A model summarizing the modulation of the photosynthetic apparatus during the acclimation response to light of different spectral quality is proposed. Our study suggests that toggling between alternative organizations of photosynthetic apparatus and distinct cell morphologies underlies the remarkable acclimation capacity of diatoms.

Early dynamics of photosynthetic Lhcf2 and Lhcf15 transcription and mRNA stabilities in response to herbivory-related decadienal in Phaeodactylum tricornutum

“…Clear precedents exist for stress condition stimulation of LHC protein abundance for photoprotection such as LHCX family members in P. tricornutum 48 . LHCF15 protein was not detected under normal growth conditions but accumulated after several days under red light enriched conditions to form an additional antennae assembly 39 . LHCF15 proteins display a strongly red-shifted absorption when in oligomeric complexes and were shown to function in light harvesting to PSII with also evidence of PSI association, the latter similar to the well-known red-shifted proteins that form part of PSI antennae in higher plants 40,56 .…”

“…Lhcf15 mRNA was the sole upregulated LHCF transcript. LHCF15 mRNA is of interest as it was induced by prolonged dark and red light 14,38 and encodes a distinctive red-shifted absorbing protein 39,40 . To resolve the kinetics of DD regulation during the light cycle, a more detailed time course was carried out and fold changes relative to the 0 h time point are presented ( Fig.…”

“…Red-shifted antennae proteins have been observed especially in cyanobacteria and microalgae and they have been postulated to enable niche expansion by accessing a less utilized portion of the light spectrum for photosynthesis 57 . In ecological value, LHCF15 was postulated to confer expanded light absorption to permit growth in shaded locations depleted of main photosynthetic wavelengths by other photosynthesizing organisms in the water column or in a biofilm on a solid coastal substrate 39 . In sublethal DD conditions, we speculate that the small set of LHC mRNAs which accumulate during the early response result in higher levels of encoded proteins in support of photosynthesis and cell health.…”

Light and photosynthetic microalgae: A review of cellular- and molecular-scale optical processes

“…However, microalgae do regulate their photosynthetic apparatus as a response to light color. Exposing microalgae to red light conditions leads to slow increase in the red light absorption (around 710 nm) and in reorganization of the thylakoid membrane architecture (Herbstova et al 2017;Kotabova et al 2014). Also, in a study by Valle et al the in-vivo fluorescence excitation spectrum was dependent on the color of the incident light after more than 30 minutes exposure, which suggests color-dependent energy transfer efficiency for diatom Phaeodactylum tricornutum (Valle et al 2014).…”

Rapid regulation of excitation energy in two pennate diatoms from contrasting light climates

“…The ratio of F689:F696 varied between Nitzschia cultures (data not shown). Dense, intermittent light:dark, or red light grown cultures of P. tricornutum exhibit a strong emission peak at ~ 710 nm (Lavaud and Lepetit 2013 ; Herbstová et al 2015 , 2017 ), with F710:F687 ratio positively correlating with NPQ capacity (Lavaud and Lepetit 2013 ). The F710 emitter serves as an antenna for PSII and was located within a red-shifted FCP composed of oligomeric Lhcf15 (Herbstová et al 2015 , 2017 ).…”