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.

Faculty of Science University of South Bohemia Branišovská 1760 37005 České Budějovice Czech Republic

Institute of Microbiology Algatech Centre CAS Opatovický mlýn 379 81 Třeboň Czech Republic

Institute of Plant Molecular Biology Biology Centre Czech Academy of Sciences Branišovská 31 37005 České Budějovice Czech Republic

Zobrazit více v PubMed

Falkowski PG, Barber RT, Smetacek VV. Biogeochemical controls and feedbacks on ocean primary production. Science. 1998;281:200–207. doi: 10.1126/science.281.5374.200. PubMed DOI

Field CB, Behrenfeld MJ, Randerson JT, Falkowski PG. Primary production of the biosphere: integrating terrestrial and oceanic components. Science. 1998;281:237–240. doi: 10.1126/science.281.5374.237. PubMed DOI

Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Queguiner B. Production and dissolution of biogenic silica in the oceans: revisited global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob. Biogeochem. Cycles. 1995;9:359–372. doi: 10.1029/95GB01070. DOI

Falkowski PG, et al. The evolution of modern eukaryotic phytoplankton. Science. 2004;305:354–360. doi: 10.1126/science.1095964. PubMed DOI

De Martino A, Meichenin A, Shi J, Pan K, Bowler C. Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions. J. Phycol. 2007;43:992–1009. doi: 10.1111/j.1529-8817.2007.00384.x. DOI

Wachnicka A, Gaiser E, Boyer J. Ecology and distribution of diatoms in Biscayne Bay, Florida (USA): Implications for bioassessment and paleoenvironmental studies. Ecol. Indic. 2011;11:622–632. doi: 10.1016/j.ecolind.2010.08.008. DOI

Dring MJ. Chromatic adaptation of photosynthesis in benthic marine algae: An examination of its ecological significance using a theoretical model. Limnol. Oceanogr. 1981;26:271–284. doi: 10.4319/lo.1981.26.2.0271. DOI

Depauw FA, Rogato A, d’Alcala MR, Falciatore A. Exploring the molecular basis of responses to light in marine diatoms. J. Exp. Bot. 2012;63:1575–1591. doi: 10.1093/jxb/ers005. PubMed DOI

Valle KC, et al. System Responses to Equal Doses of Photosynthetically Usable Radiation of Blue, Green, and Red Light in the Marine Diatom Phaeodactylum tricornutum. PLos One. 2014;9:e114211. doi: 10.1371/journal.pone.0114211. PubMed DOI PMC

Fortunato AE, et al. Diatom phytochromes reveal the existence of far-red-light-based sensing in the oceans. Plant Cell. 2016;28:616–628. doi: 10.1105/tpc.15.00928. PubMed DOI PMC

Lavaud J, Strzepek RF, Kroth PG. Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol. Oceanogr. 2007;52:1188–1194. doi: 10.4319/lo.2007.52.3.1188. DOI

Barnett A, et al. Growth form defines physiological photoprotective capacity in intertidal benthic diatoms. ISME J. 2014;9:32–45. doi: 10.1038/ismej.2014.105. PubMed DOI PMC

Engelmann TW. Farbe und Assimilation. I. Assimilation findet nur in den farbstoffhaltigen Plasmatheilchen statt. II. Näherer Zusammenhang zwischen Lichtabsorbtion und Assimilation. III. Weitere folgerungen Bot. 1883;41:1–29.

Mouget J-L, Rosa P, Tremblin G. Acclimation of Haslea ostrearia to light of different spectral qualities – confirmation of ‘chromatic adaptation’ in diatoms. J. Photochem. Photobiol. B. 2004;75:1–11. doi: 10.1016/j.jphotobiol.2004.04.002. PubMed DOI

Armbrust EV, et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science. 2004;306:79–86. doi: 10.1126/science.1101156. PubMed DOI

Bowler C, et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature. 2008;456:239–244. doi: 10.1038/nature07410. PubMed DOI

Costa BS, et al. Blue light is essential for high light acclimation and photoprotection in the diatom. J. Exp. Bot. 2013;64:483–493. doi: 10.1093/jxb/ers340. PubMed DOI PMC

Lepetit B, Goss R, Jakob T, Wilhelm C. Molecular dynamic of the diatom thylakoid membrane under different light conditions. Photosynth. Res. 2012;111:245–257. doi: 10.1007/s11120-011-9633-5. PubMed DOI

Nymark M, et al. An integrated analysis of molecular acclimation to high light in the marine diatom Phaeodactylum tricornutum. PLoS One. 2009;4:e7743. doi: 10.1371/journal.pone.0007743. PubMed DOI PMC

Nymark M, et al. Molecular and photosynthetic responses to prolonged darkness and subsequent acclimation to re-illumination in the diatom Phaeodactylum tricornutum. PLoS One. 2013;8:e58722. doi: 10.1371/journal.pone.0058722. PubMed DOI PMC

Lepetit B, et al. Evidence for the existence of one antenna-associated, lipid-dissolved and two protein-bound pools of diadinoxanthin cycle pigments in diatoms. Plant Physiol. 2010;154:1905–1920. doi: 10.1104/pp.110.166454. PubMed DOI PMC

Dong H-P, et al. High light stress triggers distinct proteomic responses in the marine diatom Thalassiosira pseudonana. BMC Genomics. 2016;17:994. doi: 10.1186/s12864-016-3335-5. PubMed DOI PMC

Dittami SM, et al. Chlorophyll-binding proteins revisited - a multigenic family of light-harvesting and stress proteins from a brown algal perspective. BMC Evol. Biol. 2010;10:365. doi: 10.1186/1471-2148-10-365. PubMed DOI PMC

Bína D, et al. Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. II. Biochemistry and spectroscopy. Biochim. Biophys. Acta. 2014;1837:802–810. doi: 10.1016/j.bbabio.2014.01.011. PubMed DOI

Herbstová M, et al. Molecular basis of chromatic adaptation in pennate diatom Phaeodactylum tricornutum. Biochim. Biophys. Acta. 2015;1847:534–543. doi: 10.1016/j.bbabio.2015.02.016. PubMed DOI

Fujita Y, Ohki K. On the 710 nm fluorescence emitted by the diatom Phaeodactylum tricornutum at room temperature. Plant. Cell Physiol. 2004;45:392–397. doi: 10.1093/pcp/pch043. PubMed DOI

Bína D, Herbstová M, Gardian Z, Vácha F, Litvín R. Novel structural aspect of the diatom thylakoid membrane: lateral segregation of photosystem I under red-enhanced illumination. Sci. Rep. 2016;6:25583. doi: 10.1038/srep25583. PubMed DOI PMC

Grouneva I, Rokka A, Aro E-M. The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J. Prot. Res. 2011;10:5338–5353. doi: 10.1021/pr200600f. PubMed DOI

Nagao R, et al. Comparison of oligomeric states and polypeptide compositions of fucoxanthin chlorophyll a/c-binding protein complexes among various diatom species. Photosynth. Res. 2013;117:281–288. doi: 10.1007/s11120-013-9903-5. PubMed DOI

De Martino A, et al. Physiological and molecular evidence that environmental changes elicit morphological interconversion in the model diatom Phaeodactylum tricornutum. Protist. 2011;162:462–481. doi: 10.1016/j.protis.2011.02.002. PubMed DOI

Kotabová E, et al. Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. I. Physiological relevance and functional connection to Photosystems. Biochim. Biophys. Acta. 2014;1837:734–743. doi: 10.1016/j.bbabio.2014.01.012. PubMed DOI

Joshi-Deo J, et al. Characterization of a trimeric light-harvesting complex in the diatom Phaeodactylum tricornutum built of FcpA and FcpE proteins. J. Exp. Bot. 2010;61:3079–3087. doi: 10.1093/jxb/erq136. PubMed DOI PMC

Gundermann K, Schmidt M, Weisheit W, Mittag M, Buechel C. Identification of several sub-populations in the pool of light harvesting proteins in the pennate diatom Phaeodactylum tricornutum. Biochim. Biophys. Acta. 2012;1827:303–310. doi: 10.1016/j.bbabio.2012.10.017. PubMed DOI

Lepetit B, et al. Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum. Biochemistry. 2007;46:9813–9822. doi: 10.1021/bi7008344. PubMed DOI

Gardian Z, Litvín R, Bína D, Vácha F. Supramolecular organization of fucoxanthin–chlorophyll proteins in centric and pennate diatoms. Photosynth. Res. 2014;121:79–86. doi: 10.1007/s11120-014-9998-3. PubMed DOI

Kühl M, et al. A niche for cyanobacteria containing chlorophyll d. Nature. 2005;433:820. doi: 10.1038/433820a. PubMed DOI

Croce R, van Amerongen H. Natural strategies for photosynthetic light harvesting. Nature Chem. Biol. 2014;10:492–501. doi: 10.1038/nchembio.1555. PubMed DOI

Li Y, Chen M. Novel chlorophylls and new directions in photosynthesis research. Funct. Plant Biol. 2015;42:493–501. doi: 10.1071/FP14350. PubMed DOI

Fork DC, Larkum AWD. Light harvesting in the green alga Ostreobium sp., a coral symbiont adapted to extreme shade. Mar. Biol. 1989;103:381–385. doi: 10.1007/BF00397273. DOI

Koehne B, Elli G, Jenings RC, Wilhelm C, Trissl HW. Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp. Biochim. Biophys. Acta. 1999;1412:94–107. doi: 10.1016/S0005-2728(99)00061-4. PubMed DOI

Wilhelm C, Jakob T. Uphill energy transfer from long-wavelength absorbing chlorophylls to PSII in Ostreobium sp. is functional in carbon assimilation. Photosynth. Res. 2006;87:323–329. doi: 10.1007/s11120-005-9002-3. PubMed DOI

Sundarabalan B, Shanmugam P. Modelling of underwater light fields in turbid and eutrophic waters: application and validation with experimental data. Ocean Sci. 2015;11:33–52. doi: 10.5194/os-11-33-2015. DOI

ASTM G173-03(2012), Standard Tables for Reference Solar Spectral Irradiances: Direct Normal and Hemispherical on 37° Tilted Surface, ASTM International, West Conshohocken, PA, 2012, http://rredc.nrel.gov/solar/spectra/am1.5/.

Buiteveld, H., Hakvoort, J. H. M. & Donze, M. The optical properties of pure water, in: J.S. Jaffe (Ed.) Ocean Optics XII, Proceedings of the Society of Photo-optical Instrumentation Engineers (SPIE), 2258, SPIE - Int. Soc. Optical Engineering, Bellingham, USA, 174–183 (1994).

Varunan T, Shanmugam P. A model for estimating size-fractioned phytoplankton absorption coefficients in coastal and oceanic waters from satellite data. Remote Sensing of Environment. 2015;158:235–254. doi: 10.1016/j.rse.2014.11.008. DOI

Lavaud J, Lepetit B. An explanation for the inter-species variability of the photoprotective non-photochemical chlorophyll fluorescence quenching in diatoms. Biochim. Biophys. Acta. 2013;1827:294–302. doi: 10.1016/j.bbabio.2012.11.012. PubMed DOI

Flori S, et al. Plastid thylakoid architecture optimizes photosynthesis in diatoms. Nat. Commun. 2017;8:15885. doi: 10.1038/ncomms15885. PubMed DOI PMC

Schägger H, Cramer WA, von Jagow G. Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 1994;217:220–230. doi: 10.1006/abio.1994.1112. PubMed DOI

Premvardhan L, Bordes L, Beer A, Büchel C, Robert B. Carotenoid structures and environments in trimeric and oligomeric fucoxanthin chlorophyll a/c2 proteins from resonance Raman spectroscopy. J. Phys. Chem. B. 2009;113:12565–12574. doi: 10.1021/jp903029g. PubMed DOI

Tichý J, et al. Light harvesting complexes of Chromera velia, photosynthetic relative of apicomplexan parasites. Biochim. Biophys. Acta. 2013;1827:723–729. doi: 10.1016/j.bbabio.2013.02.002. PubMed DOI

Eustigmatophyte model of red-shifted chlorophyll a absorption in light-harvesting complexes

Light quality, oxygenic photosynthesis and more

Red-shifted light-harvesting system of freshwater eukaryotic alga Trachydiscus minutus (Eustigmatophyta, Stramenopila)