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Coordinated rearrangements of assimilatory and storage cell compartments in a nitrogen-starving symbiotic chlorophyte cultivated under high light

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Abstract

A quantitative micromorphometric study of the cell compartment rearrangements was performed in a symbiotic chlorophyte Desmodesmus sp. 3Dp86E-1 grown on nitrogen (N) replete or N-free medium under 480 μmol PAR quanta m−2 s−1. The changes in the chloroplast, intraplastidial, and cytoplasmic inclusions induced by high light (HL) and N starvation were similar to those characteristic of free-living chlorophytes. The N-sufficient culture responded to HL by a transient swelling of the thylakoid lumen and a decline in photosynthetic efficiency followed by its recovery. In the N-starving cells, a more rapid expansion and thylakoid swelling occurred along with the irreversible decline in the photosynthetic efficiency. Differential induction of starch grains, oil bodies, and cell wall polysaccharides depending on the stress exposure and type was recorded. Tight relationships between the changes in the assimilatory and storage compartments in the stressed Desmodesmus sp. cells were revealed.

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Abbreviations

chl:

Chlorophyll

CW:

Cell wall

HL:

High light

N:

Nitrogen

Pg:

Plastoglobuli

SG:

Starch grains

TAG:

Triacylglycerines

OB:

Oil bodies

References

  • Abe J, Kubo T, Takagi Y, Saito T, Miura K, Fukuzawa H, Matsuda Y (2004) The transcriptional program of synchronous gametogenesis in Chlamydomonas reinhardtii. Curr Genet 46:304–315. doi:10.1007/s00294-004-0526-4

    Article  CAS  PubMed  Google Scholar 

  • Austin JR, Frost E, Vidi P-A, Kessler F, Staehelin LA (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18:1693–1703. doi:10.1105/tpc.105.039859

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barbato R, Friso G, Rigoni F, Dalla Vecchia F, Giacometti GM (1992) Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids. J Cell Biol 119:325–335

    Article  CAS  PubMed  Google Scholar 

  • Baulina OI (2012) Ultrastructural plasticity of cyanobacteria. Springer, Berlin

    Book  Google Scholar 

  • Berner T, Izhaki I (1994) Effect of exogenous nitrogen levels on ultrastructure of zooxanthellae from the hermatypic coral Pocillopora damicornis. Pac Sci 48:254–262

    CAS  Google Scholar 

  • Besagni C, Kessler F (2013) A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation. Planta 237:463–470. doi:10.1007/s00425-012-1813-9

    Article  CAS  PubMed  Google Scholar 

  • Cunningham A, Maas P (1978) Time lag and nutrient storage effects in the transient growth response of Chlamydomonas reinhardii in nitrogen-limited batch and continuous culture. J Gen Microbiol 104:227–231. doi:10.1099/00221287-104-2-227

    Article  Google Scholar 

  • Davidi L, Katz A, Pick U (2012) Characterization of major lipid droplet proteins from Dunaliella. Planta 236:19–33. doi:10.1007/s00425-011-1585-7

    Article  CAS  PubMed  Google Scholar 

  • de Morais MG, Costa JAV (2007) Biofixation of carbon dioxide by Spirulina sp. and Scenedesmus obliquus cultivated in a three-stage serial tubular photobioreactor. J Biotechnol 129:439–445. doi:10.1016/j.jbiotec.2007.01.009

    Article  PubMed  Google Scholar 

  • Dong H-P, Williams E, Wang D-Z, Xie Z-X, Hsia R-C, Jenck A, Halden R, Li J, Chen F, Place AR (2013) Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Plant Physiol 162:1110–1126. doi:10.1104/pp.113.214320

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dubinsky Z, Berman-Frank I (2001) Uncoupling primary production from population growth in photosynthesizing organisms in aquatic ecosystems. Aquat Sci-Res Across Boundaries 63:4–17

    Article  CAS  Google Scholar 

  • Fan J, Andre C, Xu C (2011) A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Lett 585:1985–1991. doi:10.1016/j.febslet.2011.11.001

    Article  CAS  PubMed  Google Scholar 

  • Fernandes B, Teixeira J, Dragone G, Vicente AA, Kawano S, Bišová K, Přibyl P, Zachleder V, Vítová M (2013) Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri. Bioresour Technol 144:268–274. doi:10.1016/j.biortech.2013.06.096

    Article  CAS  PubMed  Google Scholar 

  • Fisher T, Berner T, Iluz D, Dubinsky Z (1998) The kinetics of the photoacclimation response of Nannochloropsis sp. (Eustigmatophyceae): a study of changes in ultrastructure and PSU density. J Phycol 34:818–824

    Article  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • García-Ferris C, Moreno J (1994) Oxidative modification and breakdown of ribulose-1, 5-bisphosphate carboxylase/oxygenase induced in Euglena gracilis by nitrogen starvation. Planta 193:208–215

    Article  Google Scholar 

  • García-Ferris C, de los Ríos A, Ascaso C, Moreno J (1996) Correlated biochemical and ultrastructural changes in nitrogen-starved Euglena gracilis. J Phycol 32:953–963. doi:10.1111/j.0022-3646.1996.00953.x

    Article  Google Scholar 

  • Geyer G (1973) Ultrahistochemie. Histochemische Arbeitsvorschriften für die Electronmikroskopie. Veb Gustav Fischer Verlag, Jena

    Google Scholar 

  • Goncalves EC, Johnson JV, Rathinasabapathi B (2013) Conversion of membrane lipid acyl groups to triacylglycerol and formation of lipid bodies upon nitrogen starvation in biofuel green algae Chlorella UTEX29. Planta 238:895–906. doi:10.1007/s00425-013-1946-5

    Article  CAS  PubMed  Google Scholar 

  • Goodson C, Roth R, Wang ZT, Goodenough U (2011) Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost. Eukaryot Cell 10:1592–1606. doi:10.1128/EC.05242-11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gorelova O, Kosevich I, Baulina O, Fedorenko T, Torshkhoeva A, Lobakova E (2009) Associations between the White Sea invertebrates and oxygen-evolving phototrophic microorganisms. Mosc Univ Biol Sci Bull 64:16–22

    Article  Google Scholar 

  • Gorelova O, Baulina O, Solovchenko A, Fedorenko T, Kravtsova T, Chivkunova O, Koksharova O, Lobakova E (2012) Green microalgae from associations with White Sea invertebrates. Microbiol (Mikrobiologiya) 81:505–507. doi:10.1134/S002626171204008X

    Article  CAS  Google Scholar 

  • Guschina IA, Harwood JL (2009) Algal lipids and effect of the environment on their biochemistry. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, Heidelberg, pp 1–24

    Chapter  Google Scholar 

  • Hockin NL, Mock T, Mulholland F, Kopriva S, Malin G (2012) The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiol 158:299–312. doi:10.1104/pp.111.184333

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hüner NP, Bode R, Dahal K, Hollis L, Rosso D, Krol M, Ivanov AG (2012). Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited. Front Plant Sci 3: article 255. doi: 10.3389/fpls.2012.00255

  • Johnson MP, Brain AP, Ruban AV (2011) Changes in thylakoid membrane thickness associated with the reorganization of photosystem II light harvesting complexes during photoprotective energy dissipation. Plant Signal Behav 6:1386–1390. doi:10.4161/psb.6.9.16503

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kates M (1986) Techniques of lipidology: Isolation, analysis and identification of lipids. Elsevier, Amsterdam

    Google Scholar 

  • Khozin-Goldberg I, Shrestha P, Cohen Z (2005) Mobilization of arachidonyl moieties from triacylglycerols into chloroplastic lipids following recovery from nitrogen starvation of the microalga Parietochloris incisa. Biochim Biophys Acta 1738:63–71. doi:10.1016/j.bbalip.2005.09.005

    Article  CAS  PubMed  Google Scholar 

  • Khozin-Goldberg I, Solovchenko A, Pal D, Cohen Z, Boussiba S (2013) Omega-3 and omega-6 LC-PUFA from photosynthetic microalgae: studies on Parietochloris incisa and Nannochloropsis sp. In: Catala A (ed) Polyunsaturated fatty acids: sources, antioxidant properties and health benefits. Nova Science Publishers, Hauppauge, pp 1–22

    Google Scholar 

  • Li Y, Han D, Sommerfeld M, Hu Q (2011) Photosynthetic carbon partitioning and lipid production in the oleaginous microalga Pseudochlorococcum sp. (Chlorophyceae) under nitrogen-limited conditions. Bioresour Technol 102:123–129. doi:10.1016/j.biortech.2010.06.036

    Article  CAS  PubMed  Google Scholar 

  • Li X, Moellering ER, Liu B, Johnny C, Fedewa M, Sears BB, Kuo M-H, Benning C (2012) A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24:4670–4686. doi:10.1105/tpc.112.105106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lourenço SO, Barbarino E, Marquez UML, Aidar E (1998) Distribution of intracellular nitrogen in marine microalgae: basis for the calculation of specific nitrogen-to-protein conversion factors. J Phycol 34:798–811

    Article  Google Scholar 

  • Majeran W, Olive J, Drapier D, Vallon O, Wollman F-A (2001) The light sensitivity of ATP synthase mutants of Chlamydomonas reinhardtii. Plant Physiol 126:421–433. doi:10.1104/pp.126.1.421

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson G (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668. doi:10.1093/jexbot/51.345.659

    Article  CAS  PubMed  Google Scholar 

  • McKay RML, Gibbs Sarah P, Vaughn KC (1991) RuBisCo activase is present in the pyrenoid of green algae. Protoplasma 162:38–45

    Article  CAS  Google Scholar 

  • Merzlyak M, Chivkunova O, Gorelova O, Reshetnikova I, Solovchenko A, Khozin-Goldberg I, Cohen Z (2007) Effect of nitrogen starvation on optical properties, pigments, and arachidonic acid content of the unicellular green alga Parietochloris incisa (Trebouxiophyceae, Chlorophyta). J Phycol 43:833–843. doi:10.1111/j.1529-8817.2007.00375.x

    Article  CAS  Google Scholar 

  • Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochem 75:50–59. doi:10.1016/j.phytochem.2011.12.007

    Article  CAS  Google Scholar 

  • Muller-Parker G, Lee KW, Cook CB (1996) Changes in the ultrastructure of symbiotic zooxanthellae (Symbiodinium sp., Dinophyceae) in fed and starved sea anemones maintained under high and low light. J Phycol 32:987–994

    Article  Google Scholar 

  • Nagy G, Ünnep R, Zsiros O, Tokutsu R, Takizawa K, Porcar L, Moyet L, Petroutsos D, Garab G, Finazzi G (2014) Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. PNAS 111:5042–5047. doi:10.1073/pnas.1322494111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nguyen HM, Baudet M, Cuiné S, Adriano JM, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11:4266–4273. doi:10.1002/pmic.201100114

    Article  CAS  PubMed  Google Scholar 

  • Přibyl P, Cepák V, Zachleder V (2012) Production of lipids in 10 strains of Chlorella and Parachlorella, and enhanced lipid productivity in Chlorella vulgaris. Appl Microbiol Biotechnol 94:549–561. doi:10.1007/s00253-012-3915-5

    Article  PubMed  Google Scholar 

  • Přibyl P, Cepák V, Zachleder V (2013) Production of lipids and formation and mobilization of lipid bodies in Chlorella vulgaris. J Appl Phycol 25:545–553. doi:10.1007/s10811-012-9889-y

    Article  Google Scholar 

  • Reynolds E (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rhiel E, Mörschel E, Wehrmeyer W (1985) Correlation of pigment deprivation and ultrastructural organization of thylakoid membranes in Cryptomonas maculata following nutrient deficiency. Protoplasma 129:62–73

    Article  CAS  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61. doi:10.1099/00221287-111-1-1

    Article  Google Scholar 

  • Roessler PG (1988) Effects of silicon deficiency on lipid composition and metabolism in the diatom Cyclotella cryptica. J Phycol 24:394–400. doi:10.1111/j.1529-8817.1988.tb04482.x

    Article  CAS  Google Scholar 

  • Simionato D, Block MA, La Rocca N, Jouhet J, Maréchal 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. doi:10.1128/EC.00363-12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sinetova M, Markelova A, Los D (2006) The effect of nitrogen starvation on the ultrastructure and pigment composition of chloroplasts in the acidothermophilic microalga Galdieria sulphuraria. Russ J Plant Physiol 53:153–162. doi:10.1134/S1021443706020026

    Article  CAS  Google Scholar 

  • Skjånes K, Rebours C, Lindblad P (2013) Potential for green microalgae to produce hydrogen, pharmaceuticals and other high value products in a combined process. Crit Rev Biotechnol 33:172–215. doi:10.3109/07388551.2012.681625

    Article  PubMed Central  PubMed  Google Scholar 

  • Solovchenko A (2012) Physiological role of neutral lipid accumulation in eukaryotic microalgae under stresses. Russ J Plant Physiol 59:167–176. doi:10.1134/S1021443712020161

    Article  CAS  Google Scholar 

  • Solovchenko A, Khozin-Goldberg I, Cohen Z, Merzlyak M (2009) Carotenoid-to-chlorophyll ratio as a proxy for assay of total fatty acids and arachidonic acid content in the green microalga Parietochloris incisa. J Appl Phycol 21:361–366. doi:10.1134/S1021443713030138

    Article  CAS  Google Scholar 

  • Solovchenko A, Merzlyak M, Khozin-Goldberg I, Cohen Z, Boussiba S (2010) Coordinated carotenoid and lipid syntheses induced in Parietochloris incisa (Chlorophyta, Trebouxiophyceae) mutant deficient in Δ5 desaturase by nitrogen starvation and high light. J Phycol 46:763–772. doi:10.1111/j.1529-8817.2010.00849.x

    Article  CAS  Google Scholar 

  • Solovchenko A, Khozin-Goldberg I, Recht L, Boussiba S (2011) Stress-induced changes in optical properties, pigment and fatty acid content of Nannochloropsis sp.: implications for non-destructive assay of total fatty acids. Mar Biotechnol 13:527–535. doi:10.1007/s10126-010-9323-x

    Article  CAS  PubMed  Google Scholar 

  • Solovchenko A, Chivkunova O, Semenova L, Selyakh I, Shcherbakov P, Karpova E, Lobakova E (2013a) Stress-induced changes in pigment and fatty acid content in the microalga Desmodesmus sp.isolated from a White Sea hydroid. Russ J Plant Physiol 60:313–321

    Article  CAS  Google Scholar 

  • Solovchenko A, Solovchenko O, Khozin-Goldberg I, Didi-Cohen S, Pal D, Cohen Z, Boussiba S (2013b) Probing the effects of high-light stress on pigment and lipid metabolism in nitrogen-starving microalgae by measuring chlorophyll fluorescence transients: studies with a Δ5 desaturase mutant of Parietochloris incisa (Chlorophyta, Trebouxiophyceae). Algal Res 2:175–182. doi:10.1016/j.algal.2013.01.010

    Article  Google Scholar 

  • Subramanian S, Barry AN, Pieris S, Sayre RT (2013) Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production. Biotechnol Biofuels 6: article 150. http://www.biotechnologyforbiofuels.com/content/6/1/1

  • Topf J, Gong H, Timberg R, Mets L, Ohad I (1992) Thylakoid membrane energization and swelling in photoinhibited Chlamydomonas cells is prevented in mutants unable to perform cyclic electron flow. Photosynth Res 32:59–69

    Article  CAS  PubMed  Google Scholar 

  • Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8:1856–1868. doi:10.1128/EC.00272-09

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wellburn A (1994) The spectral determination of chlorophyll a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. doi:10.1016/S0176-1617(11)81192-2

    Article  CAS  Google Scholar 

  • Yang Z-K, Niu Y-F, Ma Y-H, Xue J, Zhang M-H, Yang W-D, Liu J-S, Lu S-H, Guan Y, Li H-Y (2013). Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation. Biotechnol Biofuels 6: article 67. http://www.biotechnologyforbiofuels.com/content/6/1/6

  • Zachleder V, Brányiková I (2014) Starch overproduction by means of algae. In: Bajpai R, Prokop A, Zappi M (eds) Algal biorefineries. Springer, Dordrecht, pp 217–240

    Chapter  Google Scholar 

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Acknowledgments

The electron microscopy part of the work was carried out at the User Facilities Center of M.V. Lomonosov Moscow State University.

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Authors and Affiliations

  1. Department of Bioengineering Faculty of Biology, Moscow State University, GSP-1, 119234, Moscow, Russia

    Olga Gorelova, Olga Baulina, Alexei Solovchenko, Irina Selyakh, Olga Chivkunova, Larisa Semenova, Pavel Scherbakov, Olga Burakova & Elena Lobakova

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  1. Olga Gorelova
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  2. Olga Baulina
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  3. Alexei Solovchenko
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  4. Irina Selyakh
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  5. Olga Chivkunova
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  7. Pavel Scherbakov
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  8. Olga Burakova
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  9. Elena Lobakova
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Correspondence to Alexei Solovchenko.

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Communicated by Erko Stackebrandt.

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Gorelova, O., Baulina, O., Solovchenko, A. et al. Coordinated rearrangements of assimilatory and storage cell compartments in a nitrogen-starving symbiotic chlorophyte cultivated under high light. Arch Microbiol 197, 181–195 (2015). https://doi.org/10.1007/s00203-014-1036-5

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