Induction of photosynthesis under anoxic condition in Thalassiosira pseudonana and Euglena gracilis: interactions between fermentation and photosynthesis.
Gain, Gwenaëlle; Berne, Nicolas; Feller, Tomet al.
2023 • In Frontiers in Plant Science, 14, p. 1186926
[en] [en] INTRODUCTION: In their natural environment, microalgae can be transiently exposed to hypoxic or anoxic environments. Whereas fermentative pathways and their interactions with photosynthesis are relatively well characterized in the green alga model Chlamydomonas reinhardtii, little information is available in other groups of photosynthetic micro-eukaryotes. In C. reinhardtii cyclic electron flow (CEF) around photosystem (PS) I, and light-dependent oxygen-sensitive hydrogenase activity both contribute to restoring photosynthetic linear electron flow (LEF) in anoxic conditions.
METHODS: Here we analyzed photosynthetic electron transfer after incubation in dark anoxic conditions (up to 24 h) in two secondary microalgae: the marine diatom Thalassiosira pseudonana and the excavate Euglena gracilis.
RESULTS: Both species showed sustained abilities to prevent over-reduction of photosynthetic electron carriers and to restore LEF. A high and transient CEF around PSI was also observed specifically in anoxic conditions at light onset in both species. In contrast, at variance with C. reinhardtii, no sustained hydrogenase activity was detected in anoxic conditions in both species.
DISCUSSION: Altogether our results suggest that another fermentative pathway might contribute, along with CEF around PSI, to restore photosynthetic activity in anoxic conditions in E. gracilis and T. pseudonana. We discuss the possible implication of the dissimilatory nitrate reduction to ammonium (DNRA) in T. pseudonana and the wax ester fermentation in E. gracilis.
Gain, Gwenaëlle ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Berne, Nicolas ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Feller, Tom ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
Godaux, Damien ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Cenci, Ugo; Unité de Glycobiologie Structurale et Fonctionnelle, Université de Lille, CNRS, UMR8576 - UGSF, Lille, France
Cardol, Pierre ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Language :
English
Title :
Induction of photosynthesis under anoxic condition in Thalassiosira pseudonana and Euglena gracilis: interactions between fermentation and photosynthesis.
PC acknowledges financial support from the Belgian Fonds de la Recherche Scientifique F.R.S.-F.N.R.S. (PDR T.0032), the BELSPO BRAIN project B2/212/PI/PORTAL, and European Research Council (ERC, H2020-EU BEAL project 682580). PC is Senior Research Associate from Fonds de la Recherche Scientifique – FNRS. AcknowledgmentsPC acknowledges financial support from the Belgian Fonds de la Recherche Scientifique F.R.S.-F.N.R.S. (PDR T.0032), the BELSPO BRAIN project B2/212/PI/PORTAL, and European Research Council (ERC, H2020-EU BEAL project 682580). PC is Senior Research Associate from Fonds de la Recherche Scientifique – FNRS.
Alric J. (2010). Cyclic electron flow around photosystem I in unicellular green algae. Photosynth Res. 106, 47–56. doi: 10.1007/s11120-010-9566-4
Anderson S. E. Wells J. Fedorowicz A. Butterworth L. F. Meade B. Munson A. E. (2007). Evaluation of the contact and respiratory sensitization potential of volatile organic compounds generated by simulated indoor air chemistry. Toxicological Sci. 97, 355–363. doi: 10.1093/toxsci/kfm043
Atteia A. Van Lis R. Tielens A. G. M. Martin W. F. (2013). Anaerobic energy metabolism in unicellular photosynthetic eukaryotes. Biochim. Biophys. Acta 1827 (2), 210–223. doi: 10.1016/j.bbabio.2012.08.002
Bailleul B. Berne N. Murik O. Petroutsos D. Prihoda J. Tanaka A. et al. (2015). Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524 (7565), 366–369. doi: 10.1038/nature14599
Bankar S. B. Bule M. V. Singhal R. S. Ananthanarayan L. (2009). Glucose oxidase–an overview. Biotechnol. Adv. 27 (4), 489–501. doi: 10.1016/j.biotechadv.2009.04.003
Banti V. Giuntoli B. Gonzali S. Loreti E. Magneschi L. Novi G. et al. (2013). Low oxygen response mechanisms in green organisms. Int. J. Mol. Sci. 14 (3), 4734–4761. doi: 10.3390/ijms14034734
Barsanti L. Vismara R. Passarelli V. Gualtieri P.. (2001). Paramylon (β-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis. Effects of growth conditions. J. Appl. Psychol. 13, 59–65. doi: 10.1023/A:1008105416065
Burlacot A. Sawyer A. Cuiné S. Auroy-Tarrago P. Blangy S. Happe T. et al. (2018). Flavodiiron-mediated O2 photoreduction links H2 production with CO2 fixation during the anaerobic induction of photosynthesis. Plant Physiol. 177 (4), 1639–1649. doi: 10.1104/pp.18.00721
Cardol P. De Paepe R. Franck F. Forti G. Finazzi G. (2010). The onset of NPQ and ΔμH+ upon illumination of tobacco plants studied through the influence of mitochondrial electron transport. Biochim. Biophys. Acta, 1797 (2), 177–188. doi: 10.1016/j.bbabio.2009.10.002
Catalanotti C. Yang W. Posewitz M. C. Grossman A. R. (2013). Fermentation metabolism and its evolution in algae. Front. Plant Sci. 4, 150. doi: 10.3389/fpls.2013.00150
Clowez S. Godaux D. Cardol P. Wollmann F.-A. Rappaport F. (2015). The involvement of hydrogen-producing and ATP-dependent NADPH-consuming pathways in setting the redox poise in the chloroplast of Chlamydomonas reinhardtii in anoxia. J. Biol. Chem. 290 (13), 8666–88676. doi: 10.1074/jbc.M114.632588
Cournac L. Latouche G. Cerovic Z. Redding K. Ravenel J. Peltier G. (2002). In vivo interactions between photosynthesis, mitorespiration, and chlororespiration in Chlamydomonas reinhardtii. Plant Physiol. 129 (4), 1921–1928. doi: 10.1104/pp.001636
Criscuolo A. Gribaldo S. (2010). BMGE (Block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210. doi: 10.1186/1471-2148-10-210
DalCorso G. Pesaresi P. Masiero S. Aseeva E. Schunemann D. Finazzi G. et al. (2008). A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in arabidopsis. Cell 132 (2), 273–285. doi: 10.1016/j.cell.2007.12.028
Drew M. C. (1997). Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 223–250. doi: 10.1146/annurev.arplant.48.1.223
Edgar R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (5), 1792–1797. doi: 10.1093/nar/gkh340
Fan D. Y. Fitzpatrick D. Oguchi R. Ma W. Kou J. Chow W. S. et al. (2016). Obstacles in the quantification of the cyclic electron flux around Photosystem I in leaves of C3 plants. Photosynth. Res. 129, 239–251. doi: 10.1007/s11120-016-0223-4
Forestier M. King P. Zhang L. Posewitz M. Schwarzer S. Happe T. et al. (2003). Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur. J. Biochem. 270, 2750e8. doi: 10.1046/j.1432-1033.2003.03656
Gain G. Vega de Luna F. Cordoba J. Perez E. Degand H. Morsomme H. et al. (2021). Trophic state alters the mechanism whereby energetic coupling between photosynthesis and respiration occurs in Euglena gracilis. New Phytol. 232 (4), 1603–1617. doi: 10.1111/nph.17677
Genty B. Briantais J. M. Baker N. R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta Biomembr. 990, 87–92. doi: 10.1016/S0304-4165(89)80016-9
Ghysels B. Godaux D. Matagne R.-F. Cardol P. Franck F. (2013). Function of the chloroplast hydrogenase in the microalga Chlamydomonas: the role of hydrogenase and state transitions during photosynthetic activation in anaerobiosis. PloS One 8, e64161. doi: 10.1371/journal.pone.0064161
Godaux D. Bailleul B. Berne N. Cardol P. (2015). Induction of photosynthetic carbon fixation in anoxia relies on hydrogenase activity and proton-gradient regulation-Like1-Mediated cyclic electron flow in Chlamydomonas reinhardtii. Plant Physiol. 168, 648–658. doi: 10.1104/pp.15.00105
Godaux D. Emonds-Alt B. Berne N. Ghysels B. Alric J. Remacle C. et al. (2013). A novel screening method for hydrogenase-deficient mutants in Chlamydomonas reinhardtii based on in vivo chlorophyll fluorescence and photosystem II quantum yield. Int. J. Hydrogen Energy 38 (2), 1826–1836. doi: 10.1016/j.ijhydene.2012.11.081
Goldman J. Bender M. Morel F. (2017). The effects of pH and pCO2 on photosynthesis and respiration in the diatom Thalassiosira weissflogii. Photosynthesis Res. 132 (1), 83–93. doi: 10.1007/s11120-016-0330-2
Gorman D. Levine R. (1965). Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U. S. A. 54 (6), 1665–1669. doi: 10.1073/pnas.54.6.1665
Guillard R. R. L. (1975). “Culture of phytoplankton for feeding marine invertebrates,” in Culture of marine invertebrate animals. Eds. Smith W. L. Chanley M. H. (New York, USA: Plenum Press), 26–60.
Guillard R. R. L. Ryther J. H. (1962). Studies on marine planktonic diatoms i. Cyclotella nana hustedt and Detonula confervacea (Cleve) gran. Can. J. Microbiol. 8, 229–239. doi: 10.1139/m62-029
Hackstein (2015). Eukaryotic fe-hydrogenases – old eukaryotic heritage or adaptive acquisitions? Biochem. Soc. Trans. 33 (1), 47–50. doi: 10.1042/BST0330047
Hartman H. Krasna A. I. (1963). Studies on the “Adaptation” of hydrogenase in Scenedesmus. J. Biol. Chem. 238 (2), 749–757. doi: 10.1016/S0021-9258(18)81331-X
Hemschemeier A. Happe T. (2011). Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim. Biophys. Acta - Bioenergetics 1807, 919–926. doi: 10.1016/j.bbabio.2011.02.010
Hoffmeister M. Piotrowski M. Nowitzki U. Martin W. (2005). Mitochondrial trans-2-Enoyl-CoA reductase of wax ester fermentation from Euglena gracilis defines a new family of enzymes involved in lipid synthesis. J. Biol. Chem. 280 (6), 4329–44338. doi: 10.1074/jbc.M411010200
Honer Zu Bentrup K. Miczak A. Swenson D. L. Russel D. G. (1999). Characterization of activity and expression of isocitrate lyase in Mycobacterium avium and Mycobacterium tuberculosis. J. Bacteriology 181, 7161–7167. doi: 10.1128/JB.181.23.7161-7167.1999
Hutner S. Provasoli L. Schatz A. Haskins C. (1950). Some approaches to the study of the role of metals in the metabolism of microorganisms. Proc. Am. Philos. Soc. 94 (2), 152–170.
Inui H. Ishikawa T. Tamoi M. (2017). Wax ester fermentation and its application for biofuel production. Adv. Exp. Med. Biol. 979, 269–283. doi: 10.1007/978-3-319-54910-1_13
Inui H. Miyatake K. Nakano Y. Kitaoka S. (1982). Wax ester fermentation in Euglena gracilis. FEBS Lett. EBS. 150 (1), 89–93. doi: 10.1016/0014-5793(82)81310-0
Iwasaki K. Kaneko A. Tanaka Y. Ishikawa T. Noothalapati H. Yamamoto T. (2019). Visualizing wax ester fermentation in single Euglena gracilis cells by Raman microspectroscopy and multivariate curve resolution analysis. Biotechnol. Biofuels. 12 (128), 1–10. doi: 10.1186/s13068-019-1471-2
Jayakody L. N. Hayashi N. Kitagaki H. (2011). Identification of glycolaldehyde as the key inhibitor of bioethanol fermentation by yeast and genome-wide analysis of its toxicity. Biotechnol. Lett. 33, 285–292. doi: 10.1007/s10529-010-0437-z
Kamp A. de Beer D. Nitsch J. Lavik G. Stief P. (2011). Diatoms respire nitrate to survive dark and anoxic conditions. PNAS. 108, 5649–5654. doi: 10.1073/pnas.1015744108
Kamp A. Signe H. Nils R.-P. Peter S. (2015). Nitrate storage and dissimilatory nitrate reduction by eukaryotic microbes. Front. Microbiol. 6, 1492. doi: 10.3389/fmicb.2015.01492
Kamp A. Stief P. Bristow L. Thamdrup B. Glud R. (2016). Intracellular nitrate of marine diatoms as a driver of anaerobic nitrogen cycling in sinking aggregates. Front. Microbiol. 7, 1–13. doi: 10.3389/fmicb.2016.01669
Kamp A. Stief P. Knappe J. de Beer D. (2013). Response of the ubiquitous pelagic diatom Thalassiosira weissflogii to darkness and anoxia. PloS One 8, e82605. doi: 10.1371/journal.pone.0082605
Katoh K. Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 (4), 772–780. doi: 10.1093/molbev/mst010
Kessler E. (1973). Effect of anaerobiosis on photosynthetic reactions and nitrogen metabolism of algae with and without hydrogenase. Arch. Mikrobiol. 93 (2), 91-100. doi: 10.1007/BF00424940
Klughammer C. Schreiber U. (2008). Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PNAS. 1, 27–35.
Kreuzberg K. (1984). Starch fermentation via a formate producing pathway in Chlamydomonas reinhardii, chlorogonium-elongatum and chlorella-fusca. Physiologia Plantarum 61 (1), 87–94. doi: 10.1111/j.1399-3054.1984.tb06105.x
Lomas M. Glibert P. (2000). Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J. Phycol. 36, 903–913. doi: 10.1046/j.1529-8817.2000.99029.x
Lomas M. W. Rumbley C. J. Glibert P. M. (2000). Ammonium release by nitrogen sufficient diatoms in response to rapid increases in irradiance. J. Plankton Res. 22, 2351–2366. doi: 10.1093/plankt/22.12.2351
Maruyama S. Eveleigh R. J. Archibald J. M. (2013). Treetrimmer: a method for phylogenetic dataset size reduction. BMC Res. Notes 6, 145. doi: 10.1186/1756-0500-6-145
Meuser J. E. D’Adamo S. Jinkerson R. E. Mus F. Yang W. Ghirardi M. L. et al. (2012). Genetic disruption of both Chlamydomonas reinhardtii [FeFe]-hydrogenases: insight into the role of HYDA2 in H2 production. Biochem. Biophys. Res. Commun. 417 (2), 704–709. doi: 10.1016/j.bbrc.2011.12.002
Mus F. Dubini A. Seibert M. Posewitz M. C. Grossman A. R. (2007). Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J. Biol. Chem. 282 (35), 25475–25486. doi: 10.1074/jbc.M701415200
Nakazawa M. Ando H. Nishimoto A. Ohta T. Sakamoto K. Ishikawa T. et al. (2018). Anaerobic respiration coupled with mitochondrial fatty acid synthesis in wax ester fermentation by Euglena gracilis. FEBS Lett. 592 (24), 4020–4027. doi: 10.1002/1873-3468.13276
Nakazawa M. Takahashi M. Hayashi R. Matsubara Y. Kashiyama Y. Ueda M. et al. (2021). NADPH-to-NADH conversion by mitochondrial transhydrogenase is indispensable for sustaining anaerobic metabolism in Euglena gracilis. FEBS Lett. 595 (23), 2922–2930. doi: 10.1002/1873-3468.14221
Nakazawa M. Takenaka S. Ueda M. Inui H. Nakano Y. Miyatake K. (2003). Pyruvate:NADP+oxidoreductase is stabilized by its cofactor, thiamin pyrophosphate, in mitochondria of Euglena gracilis. Arch. Biochem. Biophys. 411 (2), 183–188. doi: 10.1016/S0003-9861(02)00749-X
Pedersen P. L. (2012). 3-bromopyruvate (3BP) a fast acting, promising, powerful, specific, and effective "small molecule" anti-cancer agent taken from labside to bedside: introduction to a special issue. J. Bioenerg Biomembr. 44 (1), 1–6. doi: 10.1007/s10863-012-9425-4
Pelroy R. A. Levine G. A. Bassham J. A. (1976). Kinetics of light-dark CO2 fixation and glucose assimilation by Aphanocapsa 6714. J. Bacteriol. 128 (2), 633–643. doi: 10.1128/jb.128.2.633-643.1976
Perez E. Lapaille M. Degand H. Cilibrasi L. Villavicencio- Queijeiro A. Morsomme P. et al. (2014). The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae. Mitochondrion 19 Pt B, 338–349. doi: 10.1016/j.mito.2014.02.001
Petersen J. Teich R. Brinkmann H. Cerff R. (2006). A "green" phosphoribulokinase in complex algae with red plastids: evidence for a single secondary endosymbiosis leading to haptophytes, cryptophytes, heterokonts, and dinoflagellates. J. Mol. Evol. 62 (2), 143–157. doi: 10.1007/s00239-004-0305-3
Price M. N. Dehal P. S. Arkin P. A. (2010). FastTree 2 – approximately maximum-likelihood trees for Large alignments. PloS One 5 (3), e9490. doi: 10.1371/journal.pone.0009490
Roberty S. Bailleul B. Berne N. Franck F. Cardol P. (2014). PSI mehler reaction is the main alternative photosynthetic electron pathway in symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol. 204, 81–91. doi: 10.1111/nph.12903
Rotte C. Stejskal F. Zhu G. Keithly J. S. Martin W. (2001). Pyruvate: NADP+ oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: a biochemical relic linking pyruvate metabolism in mitochondriate and amitochondriate protists. Mol. Biol. Evol. 18 (5), 710–720. doi: 10.1093/oxfordjournals.molbev.a003853
Schreiber U. Vidaver W. (1974). Chlorophyll fluorescence induction in anaerobic Scenedesmus obliquus. Biochim. Biophys. Acta 368, 97–112. doi: 10.1016/0005-2728(74)90100-5
Shimakawa G. Matsuda Y. Nakajima K. Tamoi M. Shigeoka S. Miyake C. (2017). Diverse strategies of O2 usage for preventing photo-oxidative damage under CO2 limitation during algal photosynthesis. Sci. Rep. 7, 41022. doi: 10.1038/srep41022
Shoshan M. C. (2012). 3-bromopyruvate: targets and outcomes. J. Bioenerg. Biomembr. 44, 7–15. doi: 10.1007/s10863-012-9419-2
Sicher R. C. (1984). “Glycolaldehyde inhibition of photosynthetic carbon assimilation by isolated chloroplasts and protoplasts,” in Advances in photosynthesis research: proceedings of the VIth international congress on photosynthesis, vol. 3. (Brussels, Belgium: Springer Netherlands), 413–416).
Sprowl-Tanio S. Habowski A. N. Pate K. T. McQuade M. M. Wang K. Edwards R. A. et al. (2016). Lactate/pyruvate transporter MCT-1 is a direct Wnt target that confers sensitivity to 3-bromopyruvate in colon cancer. Cancer Metab. 4, 20. doi: 10.1186/s40170-016-0159-3
Sueoka N. (1960). Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardi. Proc. Natl. Acad. Sci. USA 46 (1), 83–91. doi: 10.1073/pnas.46.1.83
Takahashi S. Murata N. (2005). Interruption of the Calvin cycle inhibits the repair of Photosystem II from photodamage. Biochim. Biophys. Acta 1708 (3), 352–261. doi: 10.1016/j.bbabio.2005.04.003
Tolleter D. Ghysels B. Alric J. Petroutsos D. Tolstygina I. Krawietz D. et al. (2011). Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell. 23 (7), 2619–2630. doi: 10.1105/tpc.111.086876
Tomita Y. Yoshioka K. Iijima H. Nakashima A. Iwata O. Suzuki K. et al. (2016). Succinate and lactate production from Euglena gracilis during dark, anaerobic conditions. Front. Microbiol. 7, 2050. doi: 10.3389/fmicb.2016.02050
Walter B. Peters J. van Beusekom J. E. E. St. John M. (2015). Interactive effects of temperature and light during deep convection: a case study on growth and condition of the diatom Thalassiosira weissflogii. ICES J. Mar. Sci. 72 (6), 2061–2071. doi: 10.1093/icesjms/fsu218
Yamada K. Nitta T. Atsuji K. Shiroyama M. Inoue K. Higuchi C. et al. (2019). Characterization of sulfur-compound metabolism underlying wax-ester fermentation in Euglena gracilis. Sci. Rep. 9, 853. doi: 10.1038/s41598-018-36600-z
