Skip to main content

Bioenergetic reprogramming plasticity under nitrogen depletion by the unicellular green alga Scenedesmus obliquus

Planta volume 247, pages 679–692 (2018)Cite this article

Abstract

Main conclusion

Simultaneous nitrogen depletion and 3,4-dichlorophenol addition induce a bioenergetic microalgal reprogramming, through strong Cyt b 6 f synthesis, that quench excess electrons from dichlorophenol’s biodegradation to an overactivated photosynthetic electron flow and H 2 -productivity.

Cellular energy management includes “rational” planning and operation of energy production and energy consumption units. Microalgae seem to have the ability to calculate their energy reserves and select the most profitable bioenergetic pathways. Under oxygenic mixotrophic conditions, microalgae invest the exogenously supplied carbon source (glucose) to biomass increase. If 3,4-dichlorophenol is added in the culture medium, then glucose is invested more to biodegradation rather than to growth. The biodegradation yield is enhanced in nitrogen-depleted conditions, because of an increase in the starch accumulation and a delay in the establishment of oxygen-depleted conditions in a closed system. In nitrogen-depleted conditions, starch cannot be invested in PSII-dependent and PSII-independent pathways for H2-production, mainly because of a strong decrease of the cytochrome b 6 f complex of the photosynthetic electron flow. For this reason, it seems more profitable for the microalga under these conditions to direct the metabolism to the synthesis of lipids as cellular energy reserves. Nitrogen-depleted conditions with exogenously supplied 3,4-dichlorophenol induce reprogramming of the microalgal bioenergetic strategy. Cytochrome b 6 f is strongly synthesized (mainly through catabolism of polyamines) to manage the electron bypass from the dichlorophenol biodegradation procedure to the photosynthetic electron flow (at the level of PQ pool) and consequently through cytochrome b 6 f and PSI to hydrogenase and H2-production. All the above showed that the selection of the appropriate cultivation conditions is the key for the manipulation of microalgal bioenergetic strategy that leads to different metabolic products and paves the way for a future microalgal “smart” biotechnology.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • Antal T, Mattila H, Hakala-Yatkin M, Tyystjarvi T, Tyystjarvi E (2010) Acclimation of photosynthesis to nitrogen deficiency in Phaseolus vulgaris. Planta 232:887–898

    CAS  Article  PubMed  Google Scholar 

  • Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125

    CAS  Article  PubMed  Google Scholar 

  • Bishop NL, Senger H (1971) Preparation and photosynthetic properties of synchronous cultures of Scenedesmus. In: San Pietro A (ed) Methods in enzymology. Academic Press, New York, pp 130–143

    Google Scholar 

  • Blaby IK, Glaesener AG, Mettler T, Fitz-Gibbon ST, Gallaher SD, Liu B, Boyle NR, Kropat J, Stitt M, Johnson S, Benning C, Pellegrini M, Casero D, Merchant SS (2013) Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell 25:4305–4323

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Article  PubMed  Google Scholar 

  • Breuer G, Martens DE, Draaisma RB, Wijffels RH, Lamers PP (2015) Photosynthetic efficiency and carbon partitioning in nitrogen-starved Scenedesmus obliquus. Algal Res 9:254–262

    Article  Google Scholar 

  • Chen CY, Yeh KL, Aisyah R, Lee DJ, Chang JS (2011) Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: a critical review. Bioresour Technol 102:71–81

    CAS  Article  PubMed  Google Scholar 

  • Davies JP, Grossman A (1998) Responses to deficiencies in macronutrients. In: Goldschmidt-Clermont M, Rochaix JD, Merchant S (eds) The molecular biology of chloroplast and mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, pp 603–635

    Google Scholar 

  • Delieu T, Walker DA (1981) Polarographic measurements of photosynthetic oxygen evolution by leaf disks. New Phytol 89:165–178

    CAS  Article  Google Scholar 

  • Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus—the protective role of polyamines. Biochim Biophys Acta 1767:272–280

    CAS  Article  PubMed  Google Scholar 

  • Draaisma RB, Wijffels RH, Slegers PM, Brentner LB, Roy A, Barbosa MJ (2013) Food commodities from microalgae. Curr Opin Biotechnol 24:169–177

    CAS  Article  PubMed  Google Scholar 

  • Evans HJ, Sorger GJ (1966) Role of mineral elements with emphasis on the univalent cations. Annu Rev Plant Physiol 17:47–76

    CAS  Article  Google Scholar 

  • Evans JR, Terashima I (1987) The effects of nitrogen nutrition on electron transport components and photosynthesis in spinach. Aust J Plant Physiol 14:59–68

    CAS  Article  Google Scholar 

  • Gaffron H (1939) Der auffalende Unterschied in der Physiologie nahe verwandter Algenstaemme nebst Bemerkungen über die Lichtatmung. Biol Zentralbl 43:402–410

    Google Scholar 

  • Gattward JN, Almeida AA, Souza JO Jr, Gomes FP, Kronzucker HJ (2012) Sodium-potassium synergism in Theobroma cacao: stimulation of photosynthesis, water-use efficiency and mineral nutrition. Physiol Plant 146:350–362

    CAS  Article  PubMed  Google Scholar 

  • Gouveia L, Oliveira AC (2008) Microalgae as a raw material for biofuels production. J Ind Microbiol Biotechnol 36:269–274

    Article  PubMed  Google Scholar 

  • Grossman A (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151:201–224

    CAS  Article  PubMed  Google Scholar 

  • Grossman AR, Croft M, Gladyshev VN, Merchant SS, Posewitz MC, Prochnik S, Spalding MH (2007) Novel metabolism in Chlamydomonas through the lens of genomics. Curr Opin Plant Biol 10:190–198

    CAS  Article  PubMed  Google Scholar 

  • Gupta KJ, Igamberdiev AU (2011) The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion 11:537–543

    CAS  Article  PubMed  Google Scholar 

  • Hemschemeier A, Fouchard S, Cournac L, Peltier G, Happe H (2008) Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks. Planta 227:397–407

    CAS  Article  PubMed  Google Scholar 

  • Ho SH, Chen CY, Chang JS (2012) Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresour Technol 113:244–252

    CAS  Article  PubMed  Google Scholar 

  • Holden M (1965) Chlorophylls. Academic Press, London

    Google Scholar 

  • Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J Cell Mol Biol 54:621–639

    CAS  Article  Google Scholar 

  • Igamberdiev AU, Hill RD (2009) Plant mitochondrial function during anaerobiosis. Ann Bot 103:259–268

    CAS  Article  PubMed  Google Scholar 

  • Ioannidis EN, Kotzabasis K (2007) Effects of polyamines on the functionality of the photosynthetic membrane in vivo and in vitro. Biochim Biophys Acta (Bioenerg) 1767:1372–1382

    CAS  Article  Google Scholar 

  • Kates M (1972) Techniques of lipidology: isolation, analysis and identification of lipids. North Holland Publishing Company, Amsterdam

    Book  Google Scholar 

  • Kotzabasis K, Christakis-Hampsas MD, Roubelakis-Angelakis KA (1993) A narrow-bore HPLC method for the identification and quantitation of free, conjugated, and bound polyamines. Anal Biochem 214:484–489

    CAS  Article  PubMed  Google Scholar 

  • Lawlor DW, Boyle FA, Young AT, Keys AJ, Kendall AC (1987) Nitrate nutrition and temperature effects on wheat: photosynthesis and photorespiration of leaves. J Exp Bot 38:393–408

    Article  Google Scholar 

  • Liu T, Li Y, Liu F, Wang C (2016) The enhanced lipid accumulation in oleaginous microalga by the potential continuous nitrogen-limitation (CNL) strategy. Bioresour Technol 203:150–159

    CAS  Article  PubMed  Google Scholar 

  • Lovell CR, Eriksen NT, Lewitus AJ, Chen YP (2002) Resistance of the marine diatom Thalassiosira sp. to toxicity of phenolic compounds. Mar Ecol. Prog Ser 229:11–18

    CAS  Article  Google Scholar 

  • Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagen. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Lütz C, Navakoudis E, Seidlitz HK, Kotzabasis K (2005) Simulated solar irradiation with enhanced UV-B adjust plastid- and thylakoid-associated polyamine changes for UV-B protection. Biochim Biophys Acta 1710:24–33

    Article  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    CAS  Article  PubMed  Google Scholar 

  • Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–136

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Merchant SS, Helmann JD (2012) Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation. Adv Microb Physiol 60:91–210

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Metcalfe LD, Schmitz AA, Pelka JR (1966) Rapid preparation of fatty acid esters from lipids for gas chromatographic analysis. Anal Chem 38:514–515

    CAS  Article  Google Scholar 

  • Navakoudis E, Lütz C, Langebartels C, Lütz-Meindl U, Kotzabasis K (2003) Ozone impact on the photosynthetic apparatus and the protective role of polyamines. Biochim Biophys Acta 1621:160–169

    CAS  Article  PubMed  Google Scholar 

  • Papazi A, Kotzabasis K (2013) “Rational” management of dichlorophenols biodegradation by the microalga Scenedesmus obliquus. PLoS One 8:e61682

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Papazi A, Andronis E, Ioannidis NE, Chaniotakis N, Kotzabasis K (2012) High yields of hydrogen production induced by meta-substituted dichlorophenols biodegradation from the green alga Scenedesmus obliquus. PLoS One 7:e49037

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Papazi A, Gjindali AI, Kastanaki E, Assimakopoulos K, Stamatakis K, Kotzabasis K (2014) Potassium deficiency, a “smart” cellular switch for sustained high yield hydrogen production by the green alga Scenedesmus obliquus. Int J Hyd Energy 39:19452–19464

    CAS  Article  Google Scholar 

  • Petroutsos D, Katapodis P, Samiotaki M, Panayotou G, Kekos D (2008) Detoxification of 2,4-dichlorophenol by the marine microalga Tetraselmis marina. Phytochemistry 69:707–714

    CAS  Article  PubMed  Google Scholar 

  • Philipps G, Happe T, Hemschemeier A (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta 235:729–745

    CAS  Article  PubMed  Google Scholar 

  • Senger H, Brinkmann G (1986) Protochlorophyll(ide) accumulation and degradation in the dark and photoconversion to chlorophyll in the light in pigment mutant C-2A’ of Scenedesmus obliquus. Physiol Plant 68:119–124

    CAS  Article  Google Scholar 

  • Sfichi L, Ioannidis N, Kotzabasis K (2004) Thylakoid-associated polyamines adjust the UV-B sensitivity of the photosynthetic apparatus by means of light-harvesting complex II changes. Photochem Photobiol 80:499–506

    CAS  Article  PubMed  Google Scholar 

  • Sfichi-Duke L, Ioannidis NE, Kotzabasis K (2008) Fast and reversible response of thylakoid-associated polyamines during and after UV-B stress: a comparative study of the wild type and a mutant lacking chlorophyll b of unicellular green alga Scenedesmus obliquus. Planta 228:341–353

    CAS  Article  PubMed  Google Scholar 

  • Siminis C, Kanellis A, Roubelakis-Angelakis K (1993) Differences in protein synthesis and peroxidase isoenzymes between recalcitrant and regenerating protoplasts. Physiol Plant 87:263–270

    CAS  Article  Google Scholar 

  • Simionato D, Block MA, La Rocca N, Jouhet J, Marechal E, Finazzi G, Morosinotto T (2013) The response of Nannochloropsis gaditana to nitrogen starvation includes de novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids, and reorganization of the photosynthetic apparatus. Eukaryot Cell 12:665–676

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-test. Photosynthesis: from light to biosphere. Kluwer Academic Press, Dordrecht, pp 977–980

    Google Scholar 

  • Terashima I, Evans JR (1988) Effects of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant Cell Physiol 29:143–155

    CAS  Google Scholar 

  • Thomas WH, Krauss RW (1955) Nitrogen metabolism in Scenedesmus as affected by environmental changes. Plant Physiol 30:113–122

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Valledor L, Furuhashi T, Recuenco-Munoz L, Wienkoop S, Weckwerth W (2014) System-level network analysis of nitrogen starvation and recovery in Chlamydomonas reinhardtii reveals potential new targets for increased lipid accumulation. Biotechnol Biofuels 7:171

    Article  PubMed  PubMed Central  Google Scholar 

  • Wei L, Derrien B, Gautier A, Houille-Vernes L, Boulouis A, Saint-Marcoux D, Malnoe A, Rappaport F, de Vitry C, Vallon O, Choquet Y, Wollman FA (2014) Nitric oxide-triggered remodeling of chloroplast bioenergetics and thylakoid proteins upon nitrogen starvation in Chlamydomonas reinhardtii. Plant Cell 26:353–372

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799

    CAS  Article  PubMed  Google Scholar 

  • Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129–139

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Yuzefovych L, Wilson G, Rachek L (2010) Different effects of oleate vs. palmitate on mitochondrial function, apoptosis, and insulin signaling in L6 skeletal muscle cells: role of oxidative stress. American journal of physiology. Endocrinol Metab 299:1096–1105

    Google Scholar 

  • Zhang L, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214:552–561

    CAS  Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Crete, Voutes University Campus, 70013, Heraklion, Crete, Greece

    Aikaterini Papazi, Anna Korelidou, Efthimios Andronis, Athina Parasyri & Kiriakos Kotzabasis

  2. Hellenic Agricultural Research Foundation “Demeter”, Fisheries Research Institute, 64007, Nea Peramos, Kavala, Greece

    Nikolaos Stamatis

Authors
  1. Aikaterini Papazi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Korelidou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Efthimios Andronis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Athina Parasyri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nikolaos Stamatis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kiriakos Kotzabasis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kiriakos Kotzabasis.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Papazi, A., Korelidou, A., Andronis, E. et al. Bioenergetic reprogramming plasticity under nitrogen depletion by the unicellular green alga Scenedesmus obliquus . Planta 247, 679–692 (2018). https://doi.org/10.1007/s00425-017-2816-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2816-3

Keywords

  • Biodegradation
  • Dichlorophenols
  • Fatty acids
  • Hydrogen production
  • Microalgae
  • Nitrogen depletion