Advertisement

Photosynthesis Research

, Volume 139, Issue 1–3, pp 553–567 | Cite as

Modulation in light utilization by a microalga Asteracys sp. under mixotrophic growth regimes

  • Akanksha Agarwal
  • Smita Patil
  • Krushna Gharat
  • Reena A. PanditEmail author
  • Arvind M. Lali
Original article

Abstract

This study is the first to explore the influence of incident light intensity on the photosynthetic responses under mixotrophic growth of microalga Asteracys sp. When grown mixotrophically, there was an enhanced regulation of non-photochemical quenching (NPQ) of the excited state of chlorophyll (Chl) a within the cells in response to white cool fluorescent high light (HL; 600 µmol photons m−2 s−1). Simultaneous measurement of reactive oxygen species (ROS) production as malondialdehyde (MDA) and ascorbate peroxidase (APX), an ROS scavenger, showed improved management of stress within mixotrophic cells under HL. Despite the observed decrease in quantum yield of photosynthesis measured through the Chl a fluorescence transient, no reduction in biomass accumulation was observed under HL for mixotrophy. However, biomass loss owing to photoinhibition was observed in cells grown phototrophically under the same irradiance. The measurements of dark recovery of NPQ suggested that “state transitions” may be partly responsible for regulating overall photosynthesis in Asteracys sp. The partitioning of photochemical and non-photochemical processes to sustain HL stress was analysed. Collectively, this study proposes that mixotrophy using glucose leads to a change in the photosynthetic abilities of Asteracys sp. while enhancing the adaptability of the alga to high irradiances.

Graphical Abstract

Keywords

Mixotrophy Chlorophyll fluorescence Photoinhibition Light intensity Microalgae 

Abbreviations

APX

Ascorbate peroxidase

CEF

Cyclic electron flow

Car

Carotenoids

Chl

Chlorophyll

DCW

Dry cell weight

EOL

Enhancement effect of light

HL

High light

LL

Low light

MDA

Malondialdehyde

MHL

Mixotrophy under high light

MLL

Mixotrophy under low light

OD

Optical density

OJIP

Chl a fluorescence transient wherein O refers to the minimum fluorescence, J and I for inflections and P for peak

PHL

Phototrophy under high light

PLL

Phototrophy under low light

PS

Photosystem

ROS

Reactive oxygen species

WW

Wet weight

Notes

Acknowledgements

This research has been supported by the Department of Biotechnology, Ministry of Science and Technology, Govt. of India and University Grants Commission (UGC), India. The authors are grateful to Govindjee for his valuable comments that helped to improve the manuscript.

Author contributions

The study was conceived and designed by AA, RP and AML. Experiments were performed by AA and KG. The data were analysed and interpreted by AA, KG and RP. Drafting and critical revision of manuscript were done by AA and RP. SP provided technical knowledge.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Albro PW, Corbett JT, Schroeder JL (1986) Application of the thiobarbiturate assay to the measurement of lipid peroxidation products in microsomes. J Biochem Biophys Methods 13:185–194.  https://doi.org/10.1016/0165-022X(86)90092-8 Google Scholar
  2. Allorent G, Tokutsu R, Roach T et al (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25:545–557.  https://doi.org/10.1105/tpc.112.108274 Google Scholar
  3. Andersen RA (2005) Algal culturing techniques, 1st edn. Elsevier, ChinaGoogle Scholar
  4. Andrade MR, Costa JAV (2007) Mixotrophic cultivation of microalga Spirulina platensis using molasses as organic substrate. Aquaculture 264:130–134.  https://doi.org/10.1016/j.aquaculture.2006.11.021 Google Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–399Google Scholar
  6. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639Google Scholar
  7. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113.  https://doi.org/10.1146/annurev.arplant.59.032607.092759 Google Scholar
  8. Baldisserotto C, Popovich C, Giovanardi M et al (2016) Photosynthetic aspects and lipid profiles in the mixotrophic alga Neochloris oleoabundans as useful parameters for biodiesel production. Algal Res 16:255–265Google Scholar
  9. Béchet Q, Muñoz R, Shilton A, Guieysse B (2013) Outdoor cultivation of temperature-tolerant Chlorella sorokiniana in a column photobioreactor under low power-input. Biotechnol Bioeng 110:118–126Google Scholar
  10. Ben-Amotz A, Avron M (1990) The biotechnology of cultivating the halotolerant alga Dunaliella. Trends Biotechnol 8:121–126Google Scholar
  11. Berteotti S, Ballottari M, Bassi R (2016) Increased biomass productivity in green algae by tuning non-photochemical quenching. Sci Rep 6:21339.  https://doi.org/10.1038/srep21339 Google Scholar
  12. Blankenship RE (2014) Molecular mechanisms of photosynthesis. Wiley-Blackwell, HobokenGoogle Scholar
  13. Bonnecarrère V, Borsani O, Díaz P et al (2011) Response to photoxidative stress induced by cold in Japonica rice is genotype dependent. Plant Sci 180:726–732Google Scholar
  14. Buch A, Archana G, Naresh Kumar G (2010) Heterologous expression of phosphoenolpyruvate carboxylase enhances the phosphate solubilizing ability of fluorescent pseudomonads by altering the glucose catabolism to improve biomass yield. Bioresour Technol 101:679–687.  https://doi.org/10.1016/j.biortech.2009.08.075 Google Scholar
  15. Ceppi MG, Oukarroum A, Çiçek N et al (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant 144:277–288Google Scholar
  16. Cheirsilp B, Torpee S (2012) Enhanced growth and lipid production of microalgae under mixotrophic culture condition: effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour Technol 110:510–516Google Scholar
  17. Chen C-Y, Yeh K-L, Aisyah R et al (2011) Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: a critical review. Bioresour Technol 102:71–81Google Scholar
  18. Collos Y, Mornet F, Sciandra A et al (1999) An optical method for the rapid measurement of micromolar concentrations of nitrate in marine phytoplankton cultures. J Appl Phycol 11:179–184.  https://doi.org/10.1023/A:1008046023487 Google Scholar
  19. Conversion LR (2014) Environmental growth chambers. http://www.egc.com/useful_info_lighting.php
  20. Cruces E, Rautenberger R, Rojas-Lillo Y et al (2017) Physiological acclimation of Lessonia spicata to diurnal changing PAR and UV radiation: differential regulation among down-regulation of photochemistry, ROS scavenging activity and phlorotannins as major photoprotective mechanisms. Photosynth Res 131:145–157.  https://doi.org/10.1007/s11120-016-0304-4 Google Scholar
  21. Cui Y, Zhang H, Lin S (2017) Enhancement of non-photochemical quenching as an adaptive strategy under phosphorus deprivation in the dinoflagellate Karlodinium veneficum. 8:1–14.  https://doi.org/10.3389/fmicb.2017.00404
  22. De-Bashan LE, Trejo A, Huss VAR et al (2008) Chlorella sorokiniana UTEX 2805, a heat and intense, sunlight-tolerant microalga with potential for removing ammonium from wastewater. Bioresour Technol 99:4980–4989Google Scholar
  23. Deblois CP, Dufresne K, Juneau P (2013) Response to variable light intensity in photoacclimated algae and cyanobacteria exposed to atrazine. Aquat Toxicol 126:77–84.  https://doi.org/10.1016/j.aquatox.2012.09.005 Google Scholar
  24. Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta (BBA)-Bioenergetics 1020:1–24Google Scholar
  25. Demmig-Adams B, Garab G, Adams III, Govindjee W (eds) (2014) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. In: Advances in photosynthesis and respiration. Springer, DordrechtGoogle Scholar
  26. Dominici P, Caffarri S, Armenante F et al (2002) Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J Biol Chem 277:22750–22758Google Scholar
  27. Dring MJ, Lüning K (1985a) Emerson enhancement effect and quantum yield of photosynthesis for marine macroalgae in simulated underwater light fields. Mar Biol 87:109–117.  https://doi.org/10.1007/BF00539418 Google Scholar
  28. Dring MJ, Lüning K (1985b) Emerson enhancement effect and quantum yield of photosynthesis for marine macroalgae in simulated underwater light fields. Mar Biol 87:109–117Google Scholar
  29. Dubinsky Z, Berner T, Aaronson S (1978) Potential of large-scale algal culture for biomass and lipid production in arid lands. In: Biotechnology and Bioengineering Symposium. City University of New York, FlushingGoogle Scholar
  30. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254Google Scholar
  31. Frank HA, Young AJ, Britton G, Cogdell RJ (eds) (1999) Incorporation of carotenoids into reaction center and light-harvesting pigment-protein complexes. In: The photochemistry of carotenoids. Springer, Dordrecht, pp 235–244Google Scholar
  32. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92.  https://doi.org/10.1016/S0304-4165(89)80016-9 Google Scholar
  33. Govindjee (1995) Sixty-three years since Kautsky: chlorophylla fluorescence. Aust J Plant Physiol 22:131–160Google Scholar
  34. Govindjee (2004) Chlorophyll a fluorescence: a bit of basics and history. In: Papageorgiou G, Govindjee (eds) Chlorophyll a fluorescence: a probe of photosynthesis. Springer, Dordrecht, pp 2–42Google Scholar
  35. Govindjee, Amesz J, Fork DC (eds) (1986) Light emission by plants and bacteria. Academic Press, OrlandoGoogle Scholar
  36. Graham JE, Bryant DA (2008) The biosynthetic pathway for synechoxanthin, an aromatic carotenoid synthesized by the euryhaline, unicellular cyanobacterium Synechococcus sp. strain PCC 7002. J Bacteriol 190:7966–7974.  https://doi.org/10.1128/JB.00985-08 Google Scholar
  37. Grama BS, Agathos SN, Jeffryes CS (2016) Balancing photosynthesis and respiration increases microalgal biomass productivity during photoheterotrophy on glycerol. ACS Sustain Chem Eng 4:1611–1618.  https://doi.org/10.1021/acssuschemeng.5b01544 Google Scholar
  38. Greenberg BM, Gaba V, Mattoo AK, Edelman M (1987) Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kd protein of photosystem II. EMBO J 6:2865–2869Google Scholar
  39. Grieco M, Tikkanen M, Paakkarinen V et al (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol 160:1896–1910Google Scholar
  40. Gwak Y, Hwang Y, Wang B et al (2014) Comparative analysis of lipidomes and transcriptomes reveal a concerted action of multiple defensive systems against photooxidative stress in Haematococcus pluvialis. J Exp Bot 65:4317–4334Google Scholar
  41. He Q, Yang H, Wu L, Hu C (2015a) Effect of light intensity on physiological changes, carbon allocation and neutral lipid accumulation in oleaginous microalgae. Bioresour Technol 191:219–228.  https://doi.org/10.1016/j.biortech.2015.05.021 Google Scholar
  42. He Q, Yang H, Xu L et al (2015b) Sufficient utilization of natural fluctuating light intensity is an effective approach of promoting lipid productivity in oleaginous microalgal cultivation outdoors. Bioresour Technol 180:79–87.  https://doi.org/10.1016/j.biortech.2014.12.088 Google Scholar
  43. Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res.  https://doi.org/10.1023/B:PRES.0000040446.87305.f4 Google Scholar
  44. Ho SH, Chen CY, Chang JS (2012) Effect of light intensity and nitrogen starvation on CO 2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresour Technol 113:244–252.  https://doi.org/10.1016/j.biortech.2011.11.133 Google Scholar
  45. Johnson MP, Davison PA, Ruban AV, Horton P (2008) The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett 582:262–266.  https://doi.org/10.1016/j.febslet.2007.12.016 Google Scholar
  46. Kalaji HM, Schansker G, Ladle RJ et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158.  https://doi.org/10.1007/s11120-014-0024-6 Google Scholar
  47. Kalaji HM, Rastogi A, Živčák M et al (2018) Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica.  https://doi.org/10.1007/s11099-018-0766-z Google Scholar
  48. Kasajima I, Takahara K, Kawai-Yamada M, Uchimiya H (2009) Estimation of the relative sizes of rate constants for chlorophyll de-excitation processes through comparison of inverse fluorescence intensities. Plant Cell Physiol 50:1600–1616Google Scholar
  49. Kasajima I, Ebana K, Yamamoto T et al (2011) Molecular distinction in genetic regulation of nonphotochemical quenching in rice. Proc Natl Acad Sci 108:13835–13840Google Scholar
  50. Kattarath SS, Ramani DG (2017) Bioproduction and characterization of silver nanoparticles from microalgae Asteracys quadricellulares, its antimicrobial and antibiofilm activities. Int J Pharma Biosci 8:714–725Google Scholar
  51. King RJ, Schramm W (1976) Photosynthetic rates of benthic marine algae in relation to light intensity and seasonal variations. Mar Biol 37:215–222Google Scholar
  52. Kirchhoff H, Horstmann S, Weis E (2000) Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants. Biochim Biophys Acta (BBA)-Bioenergetics 1459:148–168Google Scholar
  53. Klughammer C, Schreiber U (2008a) Saturation pulse method for assessment of energy conversion in PS I. PAM Appl Notes 11–14Google Scholar
  54. Klughammer C, Schreiber U (2008b) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Appl Notes 1:201–247Google Scholar
  55. Kodru S, Malavath T, Devadasu E et al (2015) The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynth Res 125:219–231.  https://doi.org/10.1007/s11120-015-0084-2 Google Scholar
  56. Kraus D (2014) Consolidated data analysis and presentation using an open-source add-in for the Microsoft Excel® spreadsheet software. Med Writ 23:25–28.  https://doi.org/10.1179/2047480613Z.000000000181 Google Scholar
  57. Lazár D (2015) Parameters of photosynthetic energy partitioning. J Plant Physiol 175:131–147.  https://doi.org/10.1016/j.jplph.2014.10.021 Google Scholar
  58. Lichtenthaler HK, Burkart S (1999) Photosynthesis and high light stress. Bulg J Plant Physiol 25:3–16Google Scholar
  59. Lichtenthaler H, Wellburn A (1983) Determinations of total carotenoids and chlorophylls b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592.  https://doi.org/10.1042/bst0110591 Google Scholar
  60. Liu X, Duan S, Li A, Sun K (2009) Effects of glycerol on the fluorescence spectra and chloroplast ultrastructure of Phaeodactylum tricornutum (Bacillariophyta). J Integr Plant Biol 51:272–278Google Scholar
  61. MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38Google Scholar
  62. Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280Google Scholar
  63. Meteonorm (2016) Meteonorm: irradiation data for every place on Earth. Meteonorm Softw. Weather Station ans Satell. NREL TMY Dataset Downloads. http://www.meteonorm.com/en/downloads/documents
  64. Mitra D, van Leeuwen J (Hans), Lamsal B (2012) Heterotrophic/mixotrophic cultivation of oleaginous Chlorella vulgaris on industrial co-products. Algal Res 1:40–48Google Scholar
  65. Mojaat M, Pruvost J, Foucault A, Legrand J (2008) Effect of organic carbon sources and Fe2+ ions on growth and β-carotene accumulation by Dunaliella salina. Biochem Eng J 39:177–184.  https://doi.org/10.1016/j.bej.2007.09.009 Google Scholar
  66. Munday JC Jr, Govindjee (1969) Fluorescence transients in Chlorella: effects of supplementary light, anaerobiosis, and methyl viologen. Prog Photosynth Res 2:913–922Google Scholar
  67. Munekage Y, Hashimoto M, Miyake C et al (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582.  https://doi.org/10.1038/nature02598 Google Scholar
  68. Murchie EH, Hubbart S, Peng S, Horton P (2005) Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development. J Exp Bot 56:449–460.  https://doi.org/10.1093/jxb/eri100 Google Scholar
  69. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880.  https://doi.org/10.1093/oxfordjournals.pcp.a076232 Google Scholar
  70. Norici A, BAZZONI A, Pugnetti A et al (2011) Impact of irradiance on the C allocation in the coastal marine diatom Skeletonema marinoi Sarno and Zingone. Plant Cell Environ 34:1666–1677Google Scholar
  71. Ozkaleli M, Erdem A (2018) Biotoxicity of titanium dioxide nanoparticles on Raphidocelis subcapitata microalgae exemplified by membrane deformation. Int J Environ Res Public Health 15:22–26.  https://doi.org/10.3390/ijerph15030416 Google Scholar
  72. Patil S, Pandit R, Lali A (2017) Responses of algae to high light exposure: prerequisite for species selection for outdoor cultivation. J Algal Biomass Util 8:75–83Google Scholar
  73. Pfündel EE, Latouche G, Meister A, Cerovic ZG (2018) Linking chloroplast relocation to different responses of photosynthesis to blue and red radiation in low and high light-acclimated leaves of Arabidopsis thaliana (L.). Photosynth Res.  https://doi.org/10.1007/s11120-018-0482-3 Google Scholar
  74. Rabinowitch E, Govindjee (1969) Photosynthesis. Wiley, New YorkGoogle Scholar
  75. Rochaix J-D (2016) The dynamics of the photosynthetic apparatus in algae. In: Applied photosynthesis-new progress. InTechGoogle Scholar
  76. Rohacek K, Bertrand M, Moreau B et al (2014) Relaxation of the non-photochemical chlorophyll fluorescence quenching in diatoms: kinetics, components and mechanisms. Philos Trans R Soc B Biol Sci.  https://doi.org/10.1098/rstb.2013.0241 Google Scholar
  77. Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916.  https://doi.org/10.1104/pp.15.01935 Google Scholar
  78. Salama AM, Pearce RS (1993) Ageing of cucumber and onion seeds: Phospholipase d, lipoxygenase activity and changes in phospholipid content. J Exp Bot 44:1253–1265.  https://doi.org/10.1093/jxb/44.8.1253 Google Scholar
  79. Sarnaik A, Pandit R, Lali A (2017) Growth engineering of Synechococcus elongatus PCC 7942 for mixotrophy under natural light conditions for improved feedstock production. Biotechnol Prog.  https://doi.org/10.1002/btpr.2490 Google Scholar
  80. Sathya S, Srisudha S (2013) Fatty acid and hydrocarbon composition in Asteracys quadricellulare (Behre). Indian J Appl Res 3:10–12Google Scholar
  81. Schansker G, Tóth SZ, Holzwarth AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the QA model. Photosynth Res 120:43–58.  https://doi.org/10.1007/s11120-013-9806-5 Google Scholar
  82. Schulze PSC, Barreira LA, Pereira HGC et al (2014) Light emitting diodes (LEDs) applied to microalgal production. Trends Biotechnol 32:422–430.  https://doi.org/10.1016/j.tibtech.2014.06.001 Google Scholar
  83. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot.  https://doi.org/10.1155/2012/217037 Google Scholar
  84. Shevela D, Bjorn L, Govindjee (2018) Photosynthesis: solar energy for life. World Scientific, SingaporeGoogle Scholar
  85. Simionato D, Basso S, Giacometti GM, Morosinotto T (2013) Optimization of light use efficiency for biofuel production in algae. Biophys Chem 182:71–78.  https://doi.org/10.1016/j.bpc.2013.06.017 Google Scholar
  86. Singh SP, Häder D-P, Sinha RP (2010) Cyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategies. Ageing Res Rev 9:79–90Google Scholar
  87. Smith RT, Bangert K, Wilkinson SJ, Gilmour DJ (2015) Synergistic carbon metabolism in a fast growing mixotrophic freshwater microalgal species Micractinium inermum. Biomass Bioenerg 82:73–86.  https://doi.org/10.1016/j.biombioe.2015.04.023 Google Scholar
  88. Solovchenko AE, Khozin-Goldberg I, Didi-Cohen S et al (2008) Effects of light intensity and nitrogen starvation on growth, total fatty acids and arachidonic acid in the green microalga Parietochloris incisa. J Appl Phycol 20:245–251Google Scholar
  89. Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B Biol 104:236–257Google Scholar
  90. Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J–I–P rise. Photosynth Res 113:15–61Google Scholar
  91. Stirbet A, Riznichenko GY, Rubin AB (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochem 79:291–323.  https://doi.org/10.1134/S0006297914040014 Google Scholar
  92. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. Probing Photosynth 445–483Google Scholar
  93. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Chlorophyll a fluorescence. Springer, The Netherlands, pp 321–362Google Scholar
  94. Subramanian G, Yadav G, Sen R (2016) Rationally leveraging mixotrophic growth of microalgae in different photobioreactor configurations for reducing the carbon footprint of an algal biorefinery: a techno-economic perspective. RSC Adv 6:72897–72904.  https://doi.org/10.1039/C6RA14611B Google Scholar
  95. Suzuki N, Koussevitzky S, Mittler RON, Miller GAD (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270Google Scholar
  96. Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60Google Scholar
  97. Tanaka K, Mitsuhashi H, Kondo N, Sugahara K (1982) Further evidence for inactivation of fructose-1, 6-bisphosphatase at the beginning of SO2 fumigation. Increase in fructose-1, 6-bisphosphate and decrease in fructose-6-phosphate in SO2-fumigated spinach leaves. Plant Cell Physiol 23:1467–1470Google Scholar
  98. Turpin DH, Elrifi IR, Birch DG, Weger HG, Holmes JJ (1988) Interactions between photosynthesis, respiration and nitrogen assimilation in microalgae. Can J Bot 66:2083–2097Google Scholar
  99. Vadiveloo A, Moheimani NR, Cosgrove JJ et al (2017) Effects of different light spectra on the growth, productivity and photosynthesis of two acclimated strains of Nannochloropsis sp. J Appl Phycol 1–10.  https://doi.org/10.1007/s10811-017-1083-9
  100. Walters RG, Horton P (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121–133Google Scholar
  101. Wang Z-H, Nie X-P, Yue W-J, Li X (2012) Physiological responses of three marine microalgae exposed to cypermethrin. Environ Toxicol 27:567–572.  https://doi.org/10.1002/tox Google Scholar
  102. Wei D, Chen F, Chen G et al (2008) Enhanced production of lutein in heterotrophic Chlorella protothecoides by oxidative stress. Sci China Ser C Life Sci 51:1088–1093.  https://doi.org/10.1007/s11427-008-0145-2 Google Scholar
  103. Wilk L, Grunwald M, Liao P-N et al (2013) Direct interaction of the major light-harvesting complex II and PsbS in nonphotochemical quenching. Proc Natl Acad Sci 110:5452–5456Google Scholar
  104. Yang C, Hua Q, Shimizu K (2000) Energetics and carbon metabolism during growth of microalgal cells under photoautotrophic, mixotrophic and cyclic light-autotrophic/dark-heterotrophic conditions. Biochem Eng J 6:87–102Google Scholar
  105. Yang S, Liu G, Meng Y et al (2014) Utilization of xylose as a carbon source for mixotrophic growth of Scenedesmus obliquus. Bioresour Technol 172:180–185Google Scholar
  106. Zhang Z, Sun D, Wu T et al (2017) The synergistic energy and carbon metabolism under mixotrophic cultivation reveals the coordination between photosynthesis and aerobic respiration in Chlorella zofingiensis. Algal Res 25:109–116.  https://doi.org/10.1016/j.algal.2017.05.007 Google Scholar
  107. Zhao X, Chen T, Feng B et al (2017) Non-photochemical quenching plays a key role in light acclimation of rice plants differing in leaf color. Front Plant Sci 7:1–17.  https://doi.org/10.3389/fpls.2016.01968 Google Scholar
  108. Zhekisheva M, Boussiba S, Khozin-Goldberg I et al (2002) Accumulation of oleic acid in Haematococcus pluvialis (Chlorophyceae) under nitrogen starvation or high light is correlated with that of astaxanthin esters. J Phycol 331:325–331Google Scholar
  109. Zhou Y, Schideman LC, Park DS et al (2015) Characterization of a Chlamydomonas reinhardtii mutant strain with improved biomass production under low light and mixotrophic conditions. Algal Res 11:134–147.  https://doi.org/10.1016/j.algal.2015.06.001 Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Akanksha Agarwal
    • 1
  • Smita Patil
    • 1
  • Krushna Gharat
    • 1
  • Reena A. Pandit
    • 1
    Email author
  • Arvind M. Lali
    • 1
    • 2
  1. 1.DBT-ICT Centre for Energy BiosciencesInstitute of Chemical TechnologyMumbaiIndia
  2. 2.Department of Chemical EngineeringInstitute of Chemical TechnologyMumbaiIndia

Personalised recommendations