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Responses of photosystems I and II of Acutodesmus obliquus to chemical stress caused by the use of recycled nutrients

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Abstract

Nutrients derived from hydrothermal gasification of Acutodesmus obliquus were tested on its biological compatibility to support growth of the same microalgae. Photosynthetic parameters of photosystems I and II (PS I and PS II) were investigated to study physiological effects on the microalgal cell. The nutrients were collected as liquid residues. Dilutions of 1:500 showed no effect on both photosystems. Lower dilutions affected PS II initially and later also PS I. Cyclic electron flow around PS I compensated for loss of electrons due to partially inhibited PS II. The highest tested concentration of liquid residue erased any photosynthetic activity of PS II after 28 min and onwards. In contrast, PS I remained active. The results suggest that PS I is less susceptible than PS II and that the mixture of chemicals in the liquid residue did not directly affect PS I but PS II. The toxicants in the residues seemed to interfere with linear electron flow of PS II even though light-driven formation of radicals and subsequent damage to one of the photosystems can be excluded as demonstrated in darkness. Lowered photosynthetic activity of PS I during actinic irradiation was caused due to lack of supply of electrons from PS II. The cyclic electron flow might play a key role in delivering the energy needed to restore PS II activity and to biodegrade the toxicants when linear electron flow failed. These negative effects of liquid residue towards microalgal cells require a remediation step for direct application of the liquid residue to substitute commercial fertilizers in microalgal mass cultures.

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References

  • Adams WW III, Muller O, Cohu CM, Demmig-Adams B (2013) May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Photosynth Res 117:31–44. doi:10.1007/s11120-013-9849-7

    Article  PubMed  CAS  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. BBA-Bioenergetics 1143:113–134. doi:10.1016/0005-2728(93)90134-2

    Article  PubMed  CAS  Google Scholar 

  • Astier C, Boussac A, Etienne AL (1984) Evidence for different binding sites on the 33-kDa protein for DCMU, atrazine and QB. FEBS Lett 167:321–326. doi:10.1016/0014-5793(84)80150-7

    Article  CAS  Google Scholar 

  • Baker NR, Bowyer JR (1994) Photoinhibition of photosynthesis: from molecular mechanisms to the field. Bios Scientific Publishers, Oxford

    Google Scholar 

  • Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol 110:689–696. doi:10.1104/pp. 110.2.689

    PubMed  CAS  PubMed Central  Google Scholar 

  • Boukis N, Galla U, D’Jesus P, Müller H, Dinjus E (2005) Gasification of wet biomass in supercritical water. Results of pilot plant experiments. In: Proceedings of the 14th European Biomass Conference, 17–21 October 2005, Paris, France. ETA-Florence Renewable Energies, Florence, Italy, p 964–967

  • Brown TM, Duan P, Savage PE (2010) Hydrothermal liquefaction and gasification of Nannochloropsis sp. Energy Fuel 24:3639–3646. doi:10.1021/ef100203u

    Article  CAS  Google Scholar 

  • Bukhov N, Carpentier R (2004) Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynth Res 82:17–33. doi:10.1023/B:PRES.0000040442.59311.72

    Article  PubMed  CAS  Google Scholar 

  • Canaani O, Schuster G, Ohad I (1989) Photoinhibition in Chlamydomonas reinhardtii: effect on state transition, intersystem energy distribution and photosystem I cyclic electron flow. Photosynth Res 20:129–146. doi:10.1007/BF00034122

    PubMed  CAS  Google Scholar 

  • Duke SO (2012) Why have no new herbicide modes of action appeared in recent years? Pest Manag Sci 68:505–512. doi:10.1002/ps.2333

    Article  PubMed  CAS  Google Scholar 

  • Endo T, Schreiber U, Asada K (1995) Suppression of quantum yield of photosystem II by hyperosmotic stress in Chlamydomonas reinhardtii. Plant Cell Physiol 36:1253–1258

    CAS  Google Scholar 

  • Foyer CH, Lelandais M, Harbinson J (1992) Control of the quantum efficiencies of photosystems I and II, electron flow, and enzyme activation following dark-to-light transitions in pea leaves. Relationship between NADP/NADPH ratios and NADP-malate dehydrogenase activation state. Plant Physiol 99:979–986. doi:10.1104/pp. 99.3.979

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fuerst EP, Norman MA (1991) Interactions of herbicides with photosynthetic electron transport. Weed Sci 39:458–464

    CAS  Google Scholar 

  • Gao S, Wang G (2012) The enhancement of cyclic electron flow around photosystem I improves the recovery of severely desiccated Porphyra yezoensis (Bangiales, Rhodophyta). J Exp Bot 63:4349–4358. doi:10.1093/jxb/ers082

    Article  PubMed  CAS  Google Scholar 

  • Gao S, Shen S, Wang G, Niu J, Lin A, Pan G (2011) PS I-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant Cell Physiol 52:885–893. doi:10.1093/pcp/pcr038

    Article  PubMed  CAS  Google Scholar 

  • Garcia Alba L, Torri C, Fabbri D, Kersten SR, Brilman DW (2013) Microalgae growth on the aqueous phase from hydrothermal liquefaction of the same microalgae. Chem Eng J 228:214–223. doi:10.1016/j.cej.2013.04.097

    Article  CAS  Google Scholar 

  • Gardner G (1989) A stereochemical model for the active site of photosystem II herbicide. Photochem Photobiol 49:331–336. doi:10.1111/j.1751-1097.1989.tb04115.x

    Article  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA-Gen Subj 990:87–92. doi:10.1016/S0304-4165(89)80016-9

    Article  CAS  Google Scholar 

  • Gilmour DJ, Hipkins MF, Webber AN, Baker NR, Boney AD (1985) The effect of ionic stress on photosynthesis in Dunaliella tertiolecta. Planta 163:250–256. doi:10.1007/BF00393515

    Article  PubMed  CAS  Google Scholar 

  • Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114. doi:10.1007/s00425-003-1077-5

    Article  PubMed  CAS  Google Scholar 

  • Hagemann M, Jeanjean R, Fulda S, Havaux M, Joset F, Erdmann N (1999) Flavodoxin accumulation contributes to enhanced cyclic electron flow around photosystem I in salt‐stressed cells of Synechocystis sp. strain PCC 6803. Physiol Plant 105:670–678. doi:10.1034/j.1399-3054.1999.105411.x

  • Hanelt D, Nultsch W (1995) Field studies of photoinhibition show non-correlations between oxygen and fluorescence measurements in the arctic red alga Palmaria palmate. J Plant Physiol 145:31–38. doi:10.1016/S0176-1617(11)81842-0

    Article  CAS  Google Scholar 

  • Havaux M (1996) Short-term responses of photosystem I to heat stress. Photosynth Res 47:85–97. doi:10.1007/BF00017756

    Article  PubMed  CAS  Google Scholar 

  • Jeanjean R, Matthijs HC, Onana B, Havaux M, Joset F (1993) Exposure of the cyanobacterium Synechocystis PCC6803 to salt stress induces concerted changes in respiration and photosynthesis. Plant Cell Physiol 34:1073–1079

    CAS  Google Scholar 

  • Joët T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol 128:760–769. doi:10.1104/pp. 010775

    Article  PubMed  PubMed Central  Google Scholar 

  • Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. BBA-Bioenergetics 376:105–115. doi:10.1016/0005-2728(75)90209-1

    Article  PubMed  CAS  Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268. doi:10.1007/BF01089043

    Article  CAS  Google Scholar 

  • Klughammer C, Schreiber U (2008a) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAN 1:27–35

    Google Scholar 

  • Klughammer C, Schreiber U (2008b) Saturation pulse method for assessment of energy conversion in PS I. PAN 1:21–24

    Google Scholar 

  • Lidholm J, Gustafsson P, Öquist G (1987) Photoinhibition of photosynthesis and its recovery in the green alga Chlamydomonas reinhardii. Plant Cell Physiol 28:1133–1140

    CAS  Google Scholar 

  • Neidhardt J, Benemann JR, Zhang L, Melis A (1998) Photosystem-II repair and chloroplast recovery from irradiance stress: relationship between chronic photoinhibition, light-harvesting chlorophyll antenna size and photosynthetic productivity in Dunaliella salina (green algae). Photosynth Res 56:175–184. doi:10.1023/A:1006024827225

    Article  CAS  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Biol 50:333–359. doi:10.1146/annurev.arplant.50.1.333

    Article  CAS  Google Scholar 

  • Papazi A, Kotzabasis K (2013) “Rational” management of dichlorophenols biodegradation by the microalga Scenedesmus obliquus. PLoS ONE 8, e61682. doi:10.1371/journal.pone.0061682

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Patzelt DJ, Hindersin S, Elsayed S, Boukis N, Kerner M, Hanelt D (2014) Hydrothermal gasification of Acutodesmus obliquus for renewable energy production and nutrient recycling of microalgal mass cultures. J Appl Phycol. doi:10.1007/s10811-014-0496-y

    Google Scholar 

  • Satoh K (1981) Fluorescence induction and activity of ferredoxin-NADP+ reductase in Bryopsis chloroplasts. BBA-Bioenergetics 638:327–333

  • Sonoike K (1996a) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247

    Article  CAS  Google Scholar 

  • Sonoike K (1996b) Degradation of psaB gene product, the reaction center subunit of photosystem I, is caused during photoinhibition of photosystem I: possible involvement of active oxygen species. Plant Sci 115:157–164. doi:10.1016/0168-9452(96)04341-5

    Article  CAS  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64. doi:10.1111/j.1399-3054.2010.01437.x

    Article  PubMed  CAS  Google Scholar 

  • Tikhonov AN (2013) pH-dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynth Res 116:511–534. doi:10.1007/s11120-013-9845-y

    Article  PubMed  CAS  Google Scholar 

  • Tjus SE, Scheller HV, Andersson B, Møller BL (2001) Active oxygen produced during selective excitation of photosystem I is damaging not only to photosystem I, but also to photosystem II. Plant Physiol 125:2007–2015. doi:10.1104/pp. 125.4.2007

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303

    Article  PubMed  Google Scholar 

  • Tyystjärvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci U S A 93:2213–2218

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang S, Zhang D, Pan X (2013) Effects of cadmium on the activities of photosystems of Chlorella pyrenoidosa and the protective role of cyclic electron flow. Chemosphere 93:230–237. doi:10.1016/j.chemosphere.2013.04.070

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the German Federal Ministry of Food and Agriculture (KF 22403411). We would like to thank Sherif Elsayed and Dr. Nikolaos Boukis (Karlsruhe Institute of Technology (KIT), Institute of Catalysis Research and Technology (IKFT), Eggenstein-Leopoldshafen, Germany, for supply with liquid residue of hydrothermal gasified A. obliquus.

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Authors and Affiliations

  1. Aquatic Ecophysiology and Phycology, University of Hamburg, Ohnhorststraße 18, 22609, Hamburg, Germany

    Dominik J. Patzelt & Dieter Hanelt

  2. Strategic Science Consult SSC Ltd., Beim Alten Gaswerk 5, 22761, Hamburg, Germany

    Dominik J. Patzelt, Stefan Hindersin & Martin Kerner

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  1. Dominik J. Patzelt
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  2. Stefan Hindersin
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  3. Martin Kerner
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Correspondence to Dominik J. Patzelt.

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This study was funded by the German Federal Ministry of Food and Agriculture (KF 22403411). All authors declare that there is no conflict of interests. This article does not contain any studies with human participants or animals performed by any of the authors.

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Patzelt, D.J., Hindersin, S., Kerner, M. et al. Responses of photosystems I and II of Acutodesmus obliquus to chemical stress caused by the use of recycled nutrients. Appl Microbiol Biotechnol 100, 361–370 (2016). https://doi.org/10.1007/s00253-015-7008-0

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  • DOI: https://doi.org/10.1007/s00253-015-7008-0

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