Assessment of photosynthesis regulation in mixotrophically cultured microalga Chlorella sorokiniana
Abstract
Mixotrophic growth of microalgae offers great potential as an efficient strategy for biofuel production. In this study, photosynthetic regulation of mixotrophically cultured Chlorella sorokiniana cells was systematically evaluated. Mixotrophic cells in the exponential growth phase showed the highest photosynthetic activity, where maximum photosynthetic O2 evolution was approximately 3- and 4-fold higher than cells in the same phase grown photoautotrophically in 1% CO2 (in air) and air, respectively. Additionally, characteristic chlorophyll fluorescence parameters demonstrated that no limitation in electron transport downstream of PSII was detected in mixotrophic cells. Up-regulation of photosynthetic activity was associated with high total ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) carboxylase activity and expression level of phosphoribulokinase (PRK). After 3 days, photosynthetic O2 evolution of mixotrophic cells that went to the stationary phase, was strongly reduced, with reduced photochemical efficiency and reorganization of the PSII complex. Simultaneously, enzymatic activity for Rubisco carboxylase and mRNA levels of Rubisco and PRK diminished. Importantly, there was almost no non-photochemical quenching for mixotrophic cells, whether grown in log or stationary phase. A decline in the quantum efficiency of PSII and an oxidized plastoquinone pool (PQ pool) was observed under N-depleted conditions during mixotrophic growth. Finally, these results demonstrate that photosynthesis is regulated differently inmore »
- Authors:
-
- Washington State Univ., Pullman, WA (United States)
- Johns Hopkins Univ., Baltimore, MD (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Energy Efficiency and Renewable Energy (EERE)
- OSTI Identifier:
- 1290785
- Alternate Identifier(s):
- OSTI ID: 1358745
- Report Number(s):
- NREL/JA-5100-66919
Journal ID: ISSN 2211-9264
- Grant/Contract Number:
- AC36-08GO28308; EE0003112
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Algal Research
- Additional Journal Information:
- Journal Volume: 19; Journal ID: ISSN 2211-9264
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; microalgae; Chlorella sorokiniana; mixotrophic; photosynthesis
Citation Formats
Li, Tingting, Kirchhoff, Helmut, Gargouri, Mahmoud, Feng, Jie, Cousins, Asaph B., Pienkos, Philip T., Gang, David R., and Chen, Shulin. Assessment of photosynthesis regulation in mixotrophically cultured microalga Chlorella sorokiniana. United States: N. p., 2016.
Web. doi:10.1016/j.algal.2016.07.012.
Li, Tingting, Kirchhoff, Helmut, Gargouri, Mahmoud, Feng, Jie, Cousins, Asaph B., Pienkos, Philip T., Gang, David R., & Chen, Shulin. Assessment of photosynthesis regulation in mixotrophically cultured microalga Chlorella sorokiniana. United States. https://doi.org/10.1016/j.algal.2016.07.012
Li, Tingting, Kirchhoff, Helmut, Gargouri, Mahmoud, Feng, Jie, Cousins, Asaph B., Pienkos, Philip T., Gang, David R., and Chen, Shulin. Tue .
"Assessment of photosynthesis regulation in mixotrophically cultured microalga Chlorella sorokiniana". United States. https://doi.org/10.1016/j.algal.2016.07.012. https://www.osti.gov/servlets/purl/1290785.
@article{osti_1290785,
title = {Assessment of photosynthesis regulation in mixotrophically cultured microalga Chlorella sorokiniana},
author = {Li, Tingting and Kirchhoff, Helmut and Gargouri, Mahmoud and Feng, Jie and Cousins, Asaph B. and Pienkos, Philip T. and Gang, David R. and Chen, Shulin},
abstractNote = {Mixotrophic growth of microalgae offers great potential as an efficient strategy for biofuel production. In this study, photosynthetic regulation of mixotrophically cultured Chlorella sorokiniana cells was systematically evaluated. Mixotrophic cells in the exponential growth phase showed the highest photosynthetic activity, where maximum photosynthetic O2 evolution was approximately 3- and 4-fold higher than cells in the same phase grown photoautotrophically in 1% CO2 (in air) and air, respectively. Additionally, characteristic chlorophyll fluorescence parameters demonstrated that no limitation in electron transport downstream of PSII was detected in mixotrophic cells. Up-regulation of photosynthetic activity was associated with high total ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) carboxylase activity and expression level of phosphoribulokinase (PRK). After 3 days, photosynthetic O2 evolution of mixotrophic cells that went to the stationary phase, was strongly reduced, with reduced photochemical efficiency and reorganization of the PSII complex. Simultaneously, enzymatic activity for Rubisco carboxylase and mRNA levels of Rubisco and PRK diminished. Importantly, there was almost no non-photochemical quenching for mixotrophic cells, whether grown in log or stationary phase. A decline in the quantum efficiency of PSII and an oxidized plastoquinone pool (PQ pool) was observed under N-depleted conditions during mixotrophic growth. Finally, these results demonstrate that photosynthesis is regulated differently in mixotrophically cultured C. sorokiniana cells than in cells grown under photoautotrophic conditions, with a particularly strong impact by nitrogen levels in the cells.},
doi = {10.1016/j.algal.2016.07.012},
journal = {Algal Research},
number = ,
volume = 19,
place = {United States},
year = {Tue Jul 19 00:00:00 EDT 2016},
month = {Tue Jul 19 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
Mixotrophic cultivation of a Chlorella sorokiniana strain for enhanced biomass and lipid production
journal, July 2014
- Li, Tingting; Zheng, Yubin; Yu, Liang
- Biomass and Bioenergy, Vol. 66
Mixotrophic growth ofChlorella sorokiniana in outdoor enclosed photobioreactor
journal, March 1996
- Lee, Yuan-Kun; Ding, Sun-Yeun; Hoe, Chye-Hock
- Journal of Applied Phycology, Vol. 8, Issue 2
Enhanced growth and lipid production of microalgae under mixotrophic culture condition: Effect of light intensity, glucose concentration and fed-batch cultivation
journal, April 2012
- Cheirsilp, Benjamas; Torpee, Salwa
- Bioresource Technology, Vol. 110
System Response of Metabolic Networks in Chlamydomonas reinhardtii to Total Available Ammonium
journal, July 2012
- Lee, Do Yup; Park, Jeong-Jin; Barupal, Dinesh K.
- Molecular & Cellular Proteomics, Vol. 11, Issue 10
Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions
journal, July 2004
- Kramer, David M.; Avenson, Thomas J.; Edwards, Gerald E.
- Trends in Plant Science, Vol. 9, Issue 7
Effects of Acetate on Facultative Autotrophy in Chlamydomonas reinhardtii Assessed by Photosynthetic Measurements and Stable Isotope Analyses
journal, April 2000
- Heifetz, Peter B.; Förster, Britta; Osmond, C. Barry
- Plant Physiology, Vol. 122, Issue 4
Dark Induction of the Non-Photochemical Quenching of Chlorophyll Fluorescence by Acetate in Chlamydomonas reinhardtii
journal, June 1996
- Endo, T.; Asada, K.
- Plant and Cell Physiology, Vol. 37, Issue 4
Effects of Light and Glycerol on the Organization of the Photosynthetic Apparatus in the Facultative Heterotroph Pyrenomonas Salina (Cryptophyceae)1
journal, October 1991
- Lewitus, Alan J.; Caron, David A.; Miller, Kenneth R.
- Journal of Phycology, Vol. 27, Issue 5
Effects of organic carbon sources on growth, photosynthesis, and respiration of Phaeodactylum tricornutum
journal, September 2008
- Liu, Xiaojuan; Duan, Shunshan; Li, Aifen
- Journal of Applied Phycology, Vol. 21, Issue 2
Interactions between organic and inorganic carbon sources during mixotrophic cultivation of Synechococcus sp.
journal, September 2004
- Kang, Ruijuan; Wang, Jing; Shi, Dingji
- Biotechnology Letters, Vol. 26, Issue 18
The two genes for the small subunit of RuBP Carboxylase/oxygenase are closely linked in Chlamydomonas reinhardtii
journal, January 1986
- Goldschmidt-Clermont, Michel
- Plant Molecular Biology, Vol. 6, Issue 1
Expression of a gene for a light-harvesting chlorophyll a/b-binding protein in Chlamydomonas reinhardtii: effect of light and acetate
journal, January 1987
- Kindle, Karen L.
- Plant Molecular Biology, Vol. 9, Issue 6
Photo- and Metabolite Regulation of the Synthesis of Ribulose Bisphosphate Carboxylase/Oxygenase and the Phycobiliproteins in the Alga Cyanidium caldarium
journal, December 1984
- Steinmüller, Klaus; Zetsche, Klaus
- Plant Physiology, Vol. 76, Issue 4
Regulation of photosynthesis in the unicellular acidophilic red alga Galdieria sulphuraria†: Regulation of photosynthesis in Galdieria
journal, June 2007
- Oesterhelt, Christine; Schmälzlin, Elmar; Schmitt, Jürgen M.
- The Plant Journal, Vol. 51, Issue 3
Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid
journal, January 1975
- Cataldo, D. A.; Maroon, M.; Schrader, L. E.
- Communications in Soil Science and Plant Analysis, Vol. 6, Issue 1
Measurement and Interpretation of Photosynthetic Light-Response Curves in Algae in the Context of Photoinhibition and diel Changes
journal, December 1993
- Henley, William J.
- Journal of Phycology, Vol. 29, Issue 6
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo
journal, June 2008
- Baker, Neil R.
- Annual Review of Plant Biology, Vol. 59, Issue 1
Structural and functional self-organization of Photosystem II in grana thylakoids
journal, September 2007
- Kirchhoff, Helmut; Haase, Winfried; Haferkamp, Silvia
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 9
Spatial variation in photosynthetic CO2 carbon and oxygen isotope discrimination along leaves of the monocot triticale (Triticum × Secale) relates to mesophyll conductance and the Péclet effect: Spatial variation in photosynthetic discrimination
journal, June 2011
- Kodama, Naomi; Cousins, Asaph; Tu, Kevin P.
- Plant, Cell & Environment, Vol. 34, Issue 9
Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana : comparisons to Nicotiana tabacum
journal, August 2013
- Walker, Berkley; Ariza, Loren S.; Kaines, Sarah
- Plant, Cell & Environment, Vol. 36, Issue 12
Regulation of starch and lipid accumulation in a microalga Chlorella sorokiniana
journal, March 2015
- Li, Tingting; Gargouri, Mahmoud; Feng, Jie
- Bioresource Technology, Vol. 180
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)
journal, May 1998
- Neidhardt, John; Benemann, John R.; Zhang, Liping
- Photosynthesis Research, Vol. 56, Issue 2, p. 175-184
Non-Photochemical Quenching. A Response to Excess Light Energy
journal, April 2001
- Müller, Patricia; Li, Xiao-Ping; Niyogi, Krishna K.
- Plant Physiology, Vol. 125, Issue 4
An ancient light-harvesting protein is critical for the regulation of algal photosynthesis
journal, November 2009
- Peers, Graham; Truong, Thuy B.; Ostendorf, Elisabeth
- Nature, Vol. 462, Issue 7272
Differential thermal effects on the energy distribution between photosystem II and photosystem I in thylakoid membranes of a psychrophilic and a mesophilic alga
journal, April 2002
- Morgan-Kiss, Rachael; Ivanov, Alexander G.; Williams, John
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1561, Issue 2
Efficient Light Harvesting by Photosystem II Requires an Optimized Protein Packing Density in Grana Thylakoids
journal, April 2010
- Haferkamp, Silvia; Haase, Winfried; Pascal, Andrew A.
- Journal of Biological Chemistry, Vol. 285, Issue 22
Coordination of photosynthetic and respiratory metabolism in Chlorella vulgaris UAM 101 in the light
journal, August 1995
- Villarejo, Arsenio; Orus, Maria Isabel; Martinez, Flor
- Physiologia Plantarum, Vol. 94, Issue 4
Uptake and Utilization of Fructose by Anabaena variabilis ATCC 29413. Effect on Respiration and Photosynthesis
journal, April 1992
- Valiente, Eduardo Fernández; Nieva, Mar; Avendaño, M. Carmen
- Plant and Cell Physiology, Vol. 33, Issue 3
Regulation of Periplasmic Carbonic Anhydrase Expression in Chlamydomonas reinhardtii by Acetate and pH
journal, September 1994
- Fett, J. P.; Coleman, J. R.
- Plant Physiology, Vol. 106, Issue 1
Thylakoid Membrane Reduction Affects the Photosystem Stoichiometry in the Cyanobacterium Synechocystis sp. PCC 6803
journal, December 2008
- Fuhrmann, Eva; Gathmann, Sven; Rupprecht, Eva
- Plant Physiology, Vol. 149, Issue 2
ATP control on state transitions in vivo in Chlamydomonas reinhardtii
journal, October 1990
- Bulté, Laurence; Gans, Pierre; Rebéillé, Fabrice
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1020, Issue 1
Mixotrophic cultivation of Chlorella vulgaris and its potential application for the oil accumulation from non-sugar materials
journal, May 2011
- Heredia-Arroyo, Tamarys; Wei, Wei; Ruan, Roger
- Biomass and Bioenergy, Vol. 35, Issue 5
Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions
journal, March 2009
- Liang, Yanna; Sarkany, Nicolas; Cui, Yi
- Biotechnology Letters, Vol. 31, Issue 7
Effects of Inorganic n Availability on Algal Photosynthesis and Carbon Metabolism
journal, February 1991
- Turpin, David H.
- Journal of Phycology, Vol. 27, Issue 1
Interactions Among Irradiance, Oxygen Evolution and Nitrite Uptake by Chlamydomonas (Chlorophyceae)1,2
journal, December 1987
- Curtis, Paul Jefferson; Megard, Robert O.
- Journal of Phycology, Vol. 23, Issue 4
Carbon metabolite feedback regulation of leaf photosynthesis and development
journal, January 2003
- Paul, M. J.; Pellny, T. K.
- Journal of Experimental Botany, Vol. 54, Issue 382
The nitrate and ammonium nitrate supply have a major influence on the response of photosynthesis, carbon metabolism, nitrogen metabolism and growth to elevated carbon dioxide in tobacco
journal, October 1999
- Geiger, M.; Haake, V.; Ludewig, F.
- Plant, Cell & Environment, Vol. 22, Issue 10
Arabidopsis Seedling Growth, Storage Lipid Mobilization, and Photosynthetic Gene Expression Are Regulated by Carbon:Nitrogen Availability
journal, February 2002
- Martin, Thomas; Oswald, Oliver; Graham, Ian A.
- Plant Physiology, Vol. 128, Issue 2
Acclimation of photosynthesis to elevated CO2 through feedback regulation of gene expression: Climate of opinion
journal, June 1996
- Van Oosten, Jean-Jacques; Besford, Robert T.
- Photosynthesis Research, Vol. 48, Issue 3
Increased capacity for photosynthesis in wheat grown at elevated CO2: the relationship between electron transport and carbon metabolism
journal, October 1995
- Habash, DimahZ.; Paul, MatthewJ.; Parry, MartinA. J.
- Planta, Vol. 197, Issue 3
Works referencing / citing this record:
Molecular basis of autotrophic vs mixotrophic growth in Chlorella sorokiniana
journal, April 2018
- Cecchin, M.; Benfatto, S.; Griggio, F.
- Scientific Reports, Vol. 8, Issue 1
Cultivation of Chlorella vulgaris in sludge extract from resorcinol-rich wastewater: the removal and inhibitory effect of sludge toxicity: Cultivation of Chlorella vulgaris in sludge extract from resorcinol-rich wastewater
journal, January 2019
- Chen, Xiurong; Zhou, Tianjun; Wang, Xiaoxiao
- Journal of Chemical Technology & Biotechnology, Vol. 94, Issue 4
Cell growth and lipid accumulation of a microalgal mutant Scenedesmus sp. Z-4 by combining light/dark cycle with temperature variation
journal, November 2017
- Ma, Chao; Zhang, Yan-Bo; Ho, Shih-Hsin
- Biotechnology for Biofuels, Vol. 10, Issue 1
Glucose addition-induced changes in the growth and chemical compositions of a freshwater microalga Chlorella kessleri: Impacts of glucose addition in Chlorella kessleri
journal, December 2018
- Deng, Xiang-Yuan; Xue, Chun-Ye; Chen, Biao
- Journal of Chemical Technology & Biotechnology, Vol. 94, Issue 4
Respirometry as a tool to quantify kinetic parameters of microalgal mixotrophic growth
journal, February 2019
- Sforza, Eleonora; Pastore, Martina; Barbera, Elena
- Bioprocess and Biosystems Engineering, Vol. 42, Issue 5