Planta

, Volume 247, Issue 3, pp 679–692 | Cite as

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

  • Aikaterini Papazi
  • Anna Korelidou
  • Efthimios Andronis
  • Athina Parasyri
  • Nikolaos Stamatis
  • Kiriakos Kotzabasis
Original Article
  • 92 Downloads

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.

Keywords

Biodegradation Dichlorophenols Fatty acids Hydrogen production Microalgae Nitrogen depletion 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Antal T, Mattila H, Hakala-Yatkin M, Tyystjarvi T, Tyystjarvi E (2010) Acclimation of photosynthesis to nitrogen deficiency in Phaseolus vulgaris. Planta 232:887–898CrossRefPubMedGoogle Scholar
  2. Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125CrossRefPubMedGoogle Scholar
  3. 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 130–143Google Scholar
  4. 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 25:4305–4323CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRefPubMedGoogle Scholar
  6. Breuer G, Martens DE, Draaisma RB, Wijffels RH, Lamers PP (2015) Photosynthetic efficiency and carbon partitioning in nitrogen-starved Scenedesmus obliquus. Algal Res 9:254–262CrossRefGoogle Scholar
  7. 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 102:71–81CrossRefPubMedGoogle Scholar
  8. 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 603–635Google Scholar
  9. Delieu T, Walker DA (1981) Polarographic measurements of photosynthetic oxygen evolution by leaf disks. New Phytol 89:165–178CrossRefGoogle Scholar
  10. 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 1767:272–280CrossRefPubMedGoogle Scholar
  11. Draaisma RB, Wijffels RH, Slegers PM, Brentner LB, Roy A, Barbosa MJ (2013) Food commodities from microalgae. Curr Opin Biotechnol 24:169–177CrossRefPubMedGoogle Scholar
  12. Evans HJ, Sorger GJ (1966) Role of mineral elements with emphasis on the univalent cations. Annu Rev Plant Physiol 17:47–76CrossRefGoogle Scholar
  13. Evans JR, Terashima I (1987) The effects of nitrogen nutrition on electron transport components and photosynthesis in spinach. Aust J Plant Physiol 14:59–68CrossRefGoogle Scholar
  14. Gaffron H (1939) Der auffalende Unterschied in der Physiologie nahe verwandter Algenstaemme nebst Bemerkungen über die Lichtatmung. Biol Zentralbl 43:402–410Google Scholar
  15. 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 146:350–362CrossRefPubMedGoogle Scholar
  16. Gouveia L, Oliveira AC (2008) Microalgae as a raw material for biofuels production. J Ind Microbiol Biotechnol 36:269–274CrossRefPubMedGoogle Scholar
  17. Grossman A (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151:201–224CrossRefPubMedGoogle Scholar
  18. 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 10:190–198CrossRefPubMedGoogle Scholar
  19. Gupta KJ, Igamberdiev AU (2011) The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion 11:537–543CrossRefPubMedGoogle Scholar
  20. 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 227:397–407CrossRefPubMedGoogle Scholar
  21. 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 113:244–252CrossRefPubMedGoogle Scholar
  22. Holden M (1965) Chlorophylls. Academic Press, LondonGoogle Scholar
  23. 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 54:621–639CrossRefGoogle Scholar
  24. Igamberdiev AU, Hill RD (2009) Plant mitochondrial function during anaerobiosis. Ann Bot 103:259–268CrossRefPubMedGoogle Scholar
  25. Ioannidis EN, Kotzabasis K (2007) Effects of polyamines on the functionality of the photosynthetic membrane in vivo and in vitro. Biochim Biophys Acta (Bioenerg) 1767:1372–1382CrossRefGoogle Scholar
  26. Kates M (1972) Techniques of lipidology: isolation, analysis and identification of lipids. North Holland Publishing Company, AmsterdamCrossRefGoogle Scholar
  27. 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 214:484–489CrossRefPubMedGoogle Scholar
  28. 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 38:393–408CrossRefGoogle Scholar
  29. 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 203:150–159CrossRefPubMedGoogle Scholar
  30. 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 229:11–18CrossRefGoogle Scholar
  31. Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagen. J Biol Chem 193:265–275PubMedGoogle Scholar
  32. 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 1710:24–33CrossRefPubMedGoogle Scholar
  33. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  34. Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 122:127–136CrossRefPubMedPubMedCentralGoogle Scholar
  36. Merchant SS, Helmann JD (2012) Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation. Adv Microb Physiol 60:91–210CrossRefPubMedPubMedCentralGoogle Scholar
  37. Metcalfe LD, Schmitz AA, Pelka JR (1966) Rapid preparation of fatty acid esters from lipids for gas chromatographic analysis. Anal Chem 38:514–515CrossRefGoogle Scholar
  38. 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 1621:160–169CrossRefPubMedGoogle Scholar
  39. Papazi A, Kotzabasis K (2013) “Rational” management of dichlorophenols biodegradation by the microalga Scenedesmus obliquus. PLoS One 8:e61682CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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:e49037CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 39:19452–19464CrossRefGoogle Scholar
  42. Petroutsos D, Katapodis P, Samiotaki M, Panayotou G, Kekos D (2008) Detoxification of 2,4-dichlorophenol by the marine microalga Tetraselmis marina. Phytochemistry 69:707–714CrossRefPubMedGoogle Scholar
  43. Philipps G, Happe T, Hemschemeier A (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta 235:729–745CrossRefPubMedGoogle Scholar
  44. 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 68:119–124CrossRefGoogle Scholar
  45. 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 80:499–506CrossRefPubMedGoogle Scholar
  46. 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 228:341–353CrossRefPubMedGoogle Scholar
  47. Siminis C, Kanellis A, Roubelakis-Angelakis K (1993) Differences in protein synthesis and peroxidase isoenzymes between recalcitrant and regenerating protoplasts. Physiol Plant 87:263–270CrossRefGoogle Scholar
  48. 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 12:665–676CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 977–980Google Scholar
  50. Terashima I, Evans JR (1988) Effects of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant Cell Physiol 29:143–155Google Scholar
  51. Thomas WH, Krauss RW (1955) Nitrogen metabolism in Scenedesmus as affected by environmental changes. Plant Physiol 30:113–122CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 7:171CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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 26:353–372CrossRefPubMedPubMedCentralGoogle Scholar
  54. Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799CrossRefPubMedGoogle Scholar
  55. Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129–139CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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 299:1096–1105Google Scholar
  57. Zhang L, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214:552–561CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Aikaterini Papazi
    • 1
  • Anna Korelidou
    • 1
  • Efthimios Andronis
    • 1
  • Athina Parasyri
    • 1
  • Nikolaos Stamatis
    • 2
  • Kiriakos Kotzabasis
    • 1
  1. 1.Department of BiologyUniversity of CreteHeraklionGreece
  2. 2.Hellenic Agricultural Research Foundation “Demeter”Fisheries Research InstituteNea Peramos, KavalaGreece

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