Photosynthetica 2023, 61(4):425-431 | DOI: 10.32615/ps.2023.032

Influence of reduced amounts of sulfoquinovosyl diacylglycerol on the thylakoid membranes of the diatom Thalassiosira pseudonana

T. LIEBISCH, M. BAªOGLU, S. JÄGER, C. BÜCHEL
Institute of Molecular Biosciences, Goethe University Frankfurt, Frankfurt, Germany

Diatom thylakoids contain much higher amounts of sulfoquinovosyl diacylglycerol (SQDG) than vascular plants and the hypothesis was brought forward that this relates to their special thylakoid structure. To test this hypothesis we created knock-down mutants in Thalassiosira pseudonana that exhibited a decreased SQDG content per cell. Surprisingly, the ratio between the different lipid classes did not change, pointing to strict regulation of thylakoid lipid composition. The antenna proteins, fucoxanthin-chlorophyll proteins (FCP), were reduced and photosystem (PS) I compared to PSII was increased as judged from absorbance spectra. CD spectroscopy indicated a tighter packing of chromophores. The reduction in FCP might help to avoid diametral changes in excitation energy transfer. In contrast, the increase in PSI in the mutants might counteract the diminishment of the usually huge PSI antenna. No changes in thylakoid structure were observed since the stoichiometry between different lipid classes seems to be carefully balanced.

Additional key words: algae; lipids; photosynthesis; sulfoquinovosyl diacylglycerol.

Received: May 30, 2023; Revised: July 25, 2023; Accepted: August 21, 2023; Prepublished online: September 5, 2023; Published: December 19, 2023  Show citation

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LIEBISCH, T., BAªOGLU, M., JÄGER, S., & BÜCHEL, C. (2023). Influence of reduced amounts of sulfoquinovosyl diacylglycerol on the thylakoid membranes of the diatom Thalassiosira pseudonana . Photosynthetica, 61(SPECIAL ISSUE 2023-2), 425-431. doi: 10.32615/ps.2023.032
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    References

    1. Apt K.E., Grossman A.R., Kroth-Pancic P.G.: Stable nuclear transformation of the diatom Phaeodactylum tricornutum. - Mol. Gen. Genet. 252: 572-579, 1996. Go to original source...
    2. Barka F., Angstenberger M., Ahrendt T. et al.: Identification of a triacylglycerol lipase in the diatom Phaeodactylum tricornutum. - BBA-Mol. Cell Biol. L. 1861: 239-248, 2016. Go to original source...
    3. Benning C., Beatty J.T., Prince R.C., Somerville C.R.: The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. -PNAS 90: 1561-1565, 1993. Go to original source...
    4. Benning C., Somerville C.R.: Identification of an operon involved in sulfolipid biosynthesis in Rhodobacter sphaeroides. - J. Bacteriol. 174: 6479-6487, 1992. Go to original source...
    5. Büchel C.: Fucoxanthin-chlorophyll proteins in diatoms: 18 and 19 kDa subunits assemble into different oligomeric states. - Biochemistry 42: 13027-13034, 2003. Go to original source...
    6. Büchel C., Garab G.: Organization of the pigment molecules in the chlorophyll a/c light-harvesting complex of Pleurochloris meiringensis (Xanthophyceae). Characterization with circular dichroism and absorbance spectroscopy. - J. Photoch. Photobio. B 37: 118-124, 1997. Go to original source...
    7. Büchel C., Wilhelm C., Hauswirth N., Wild A.: Evidence for a lateral heterogeneity by patch-work like areas enriched in photosystem I complexes in the three thylakoid lamellae of Pleurochloris meiringensis (Xanthophyceae). - Crypt. Bot. 2: 375-386, 1992.
    8. Essigmann B., Güler S., Narang R.A. et al.: Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. - PNAS 95: 1950-1955, 1998. Go to original source...
    9. Flori S., Jouneau P.-H., Bailleul B. et al.: Plastid thylakoid architecture optimizes photosynthesis in diatoms. - Nat. Commun. 8: 15885, 2017. Go to original source...
    10. Garab G., Kieleczawa J., Sutherland J.C. et al.: Organization of pigment-protein complexes into macrodomains in the thylakoid membranes of wild-type and chlorophyll b-less mutant of barley as revealed by circular dichroism. - Photochem. Photobiol. 54: 273-281, 1991. Go to original source...
    11. Goss R., Latowski D., Grzyb J. et al.: Lipid dependence of diadinoxanthin solubilization and de-epoxidation in artificial membrane systems resembling the lipid composition of the natural thylakoid membrane. - BBA-Biomembranes 1768: 67-75, 2007. Go to original source...
    12. Gounaris K., Barber J.: Isolation and characterization of a photosystem II reaction centre lipoprotein complex. - FEBS Lett. 188: 68-72, 1985. Go to original source...
    13. Guillard R.R.L.: Culture of phytoplankton for feeding marine invertebrates. - In: Smith W.L., Chanley M.H. (ed.): Culture of Marine Invertebrate Animals. Pp. 29-60. Springer, Boston 1975. Go to original source...
    14. Gundermann K., Büchel C.: Factors determining the fluorescence yield of fucoxanthin-chlorophyll complexes (FCP) involved in non-photochemical quenching in diatoms. - BBA-Bioenergetics 1817: 1044-1052, 2012. Go to original source...
    15. Jäger S., Büchel C.: Cation-dependent changes in the thylakoid membrane appression of the diatom Thalassiosira pseudonana. - BBA-Bioenergetics 1860: 41-51, 2019. Go to original source...
    16. Jeffrey S.W., Humphrey G.F.: New spectrometric equations for determining chlorophyll a, b, c1 and c2 in higher plants, algae and natural phytoplankton. - Biochem. Physiol. Pflanzen 167: 191-194, 1975. Go to original source...
    17. Kobayashi K.: Role of membrane glycerolipids in photosynthesis, thylakoid biogenesis and chloroplast development. - J. Plant Res. 129: 565-580, 2016. Go to original source...
    18. Lepetit B., Goss R., Jakob T., Wilhelm C.: Molecular dynamics of the diatom thylakoid membrane under different light conditions. - Photosynth. Res. 111: 245-257, 2012. Go to original source...
    19. Lepetit B., Volke D., Gilbert M. 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. 154: 1905-1920, 2010. Go to original source...
    20. Martin P., van Mooy B.A.S., Heithoff A., Dyhrman S.T.: Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana. - ISME J. 5: 1057-1060, 2011. Go to original source...
    21. Mizusawa N., Wada H.: The role of lipids in photosystem II. - BBA-Bioenergetics 1817: 194-208, 2012. Go to original source...
    22. Mulichak A.M., Theisen M.J., Essigmann B. et al.: Crystal structure of SQD1, an enzyme involved in the biosynthesis of the plant sulfolipid headgroup donor UDP-sulfoquinovose. - PNAS 96: 13097-13102, 1999. Go to original source...
    23. Nagao R., Kato K., Ifuku K. et al.: Structural basis for assembly and function of a diatom photosystem I-light-harvesting supercomplex. - Nat. Commun. 11: 2481, 2020. Go to original source...
    24. Nagao R., Kato K., Kumazawa M. et al.: Structural basis for different types of hetero-tetrameric light-harvesting complexes in a diatom PSII-FCPII supercomplex. - Nat. Commun. 13: 1764, 2022. Go to original source...
    25. Nagy G., Szabó M., Ünnep R. et al.: Modulation of the multilamellar membrane organization and of the chiral macrodomains in the diatom Phaeodactylum tricornutum revealed by small-angle neutron scattering and circular dichroism spectroscopy. - Photosynth. Res. 111: 71-79, 2012. Go to original source...
    26. Pi X., Zhao S., Wang W. et al.: The pigment-protein network of a diatom photosystem II-light-harvesting antenna supercomplex. - Science 365: eaax4406, 2019. Go to original source...
    27. Pick U., Gounaris K., Weiss M., Barber J.: Tightly bound sulpholipids in chloroplast CF0-CF1. - BBA-Bioenergetics 808: 415-420, 1985. Go to original source...
    28. Pyszniak A.M., Gibbs S.P.: Immunocytochemical localization of photosystem I and the fucoxanthin-chlorophyll a/c light-harvesting complex in the diatom Phaeodactylum tricornutum. - Protoplasma 166: 208-217, 1992. Go to original source...
    29. Sigrist M., Zwillenberg C., Giroud C. et al.: Sulfolipid associated with the light-harvesting complex associated with photosystem II apoproteins of Chlamydomonas reinhardii. - Plant Sci. 58: 15-23, 1988. Go to original source...
    30. Szabó M., Lepetit B., Goss R. et al.: Structurally flexible macro-organization of the pigment-protein complexes of the diatom Phaeodactylum tricornutum. - Photosynth. Res. 95: 237-245, 2008. Go to original source...
    31. Ünnep R., Zsiros O., Solymosi K. et al.: The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering. - BBA-Bioenergetics 1837: 1572-1580, 2014. Go to original source...
    32. Vieler A., Wilhelm C., Goss R. et al.: The lipid composition of the unicellular green alga Chlamydomonas reinhardtii and the diatom Cyclotella meneghiniana investigated by MALDI-TOF MS and TLC. - Chem. Phys. Lipids 150: 143-155, 2007. Go to original source...
    33. Xu C., Pi X., Huang Y. et al.: Structural basis for energy transfer in a huge diatom PSI-FCPI supercomplex. - Nat. Commun. 11: 5081, 2020. Go to original source...
    34. Yu B., Benning C.: Anionic lipids are required for chloroplast structure and function in Arabidopsis. - Plant J. 36: 762-770, 2003. Go to original source...
    35. Yu B., Xu C., Benning C.: Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. - PNAS 99: 5732-5737, 2002. Go to original source...

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