Effects of light intensity and carbon dioxide on lipids and fatty acids produced by Synechocystis sp. PCC6803 during continuous flow

Abstract We studied the effects of light intensity (LI) and CO2 supply on pH and total lipid production and fatty acids by Synechocystis sp. PCC6803 during continuous-flow operation of a photobioreactor having continuous nutrient supply. The temperature was fixed at 30 °C, and the LI pattern mimicked a day/night light cycle from 0 to 1920 μmol/m2 s. The CO2 supply varied from 1 to 5% v/v of total air. The total lipid content increased proportionally to LI, reaching a high content of 14% of dry weight (DW) at the highest LI at 3% CO2. In contrast, LI had no significant influence on the total fatty acid content, which was 3.4% ± 0.5% DW, measured as fatty acid methyl esters (FAMEs). Palmitic acid (C16:0) was the main fatty acid (52% of FAMEs), but γ-linolenic acid (C18:3n6) and linoleic acid (C18:2) were significant at 20% and 14% of total FAMEs, respectively. Also, α-linolenic acid (C18:3n3), oleic acid (C18:1), and palmitoleic acid (C16:1) represented 5%, 4%, and 4% of the total FAMEs, respectively. In case of C16:0, its highest content was achieved at LI of 400 to 1500 μmol/m2 s and pH media values from 7.2 to 8.8 (3% CO2). The highest formation of C16:1 and C18:1 (desirable for biodiesel production) occurred with LI up to 600 μmol/m2 s at pH 9 (3% CO2). Stearic acid (C18:0) and linoleic acid (C18:2) contents did not vary with LI or pH, but α-linolenic acid (C18:3n3) formation occurred with patterns opposite to C18:3n6, C16:0, and C16:1. LI of 400 to 1600 μmol/m2 s and pH range from 7.7 to 8.7 led to the highest values of C18:3n6 (0.8% DW), but C18:3n3 was suppressed by these conditions, supporting a desaturation pathway in Synechocystis. These results point to strategies to optimize LI, CO2, and pH, to enhance the fatty acid production profile for biofuel production.

[1]  Y. Chisti.  Biodiesel from microalgae. , 2007, Biotechnology advances.

[2]  A. Kaplan,et al.  Inorganic carbon acquisition systems in cyanobacteria , 2004, Photosynthesis Research.

[3]  Lisa Rosgaard,et al.  Bioengineering of carbon fixation, biofuels, and biochemicals in cyanobacteria and plants. , 2012, Journal of biotechnology.

[4]  Ayhan Demirbas,et al.  Algae Energy: Algae as a New Source of Biodiesel , 2010 .

[5]  B. Rittmann,et al.  Photoautotrophic nutrient utilization and limitation during semi‐continuous growth of Synechocystis sp. PCC6803 , 2010, Biotechnology and bioengineering.

[6]  J. Waterbury,et al.  Generic assignments, strain histories, and properties of pure cultures of cyanobacteria , 1979 .

[7]  T. Jenkins,et al.  Challenges with fats and fatty acid methods. , 2003, Journal of animal science.

[8]  Imogen Foubert,et al.  Optimization of an Analytical Procedure for Extraction of Lipids from Microalgae , 2012 .

[9]  Feng Chen,et al.  Fatty acid profile of the edible filamentous cyanobacterium Nostoc flagelliforme at different temperatures and developmental stages in liquid suspension culture , 2005 .

[10]  Isabel Canto de Loura,et al.  The effects of nitrogen deficiency on pigments and lipids of cyanobacteria. , 1987, Plant physiology.

[11]  L. Sherman,et al.  Global Transcriptional Response of the Alkali-Tolerant Cyanobacterium Synechocystis sp. Strain PCC 6803 to a pH 10 Environment , 2008, Applied and Environmental Microbiology.

[12]  J. Harwood,et al.  Lipids and lipid metabolism in eukaryotic algae. , 2006, Progress in lipid research.

[13]  B. Cheirsilp,et al.  Effect of nitrogen, salt, and iron content in the growth medium and light intensity on lipid production by microalgae isolated from freshwater sources in Thailand. , 2011, Bioresource technology.

[14]  K. Walsh,et al.  Effect of irradiance on fatty acid, carotenoid, total protein composition and growth of Microcystis aeruginosa , 1997 .

[15]  G. Dönmez,et al.  Microbial oil production from thermophile cyanobacteria for biodiesel production , 2011 .

[16]  Robert L. Burnap,et al.  Regulation of the carbon-concentrating mechanism in the cyanobacterium Synechocystis sp. PCC6803 in response to changing light intensity and inorganic carbon availability , 2013, Photosynthesis Research.

[17]  Jo‐Shu Chang,et al.  Perspectives on microalgal CO₂-emission mitigation systems--a review. , 2011, Biotechnology advances.

[18]  Gerhard Knothe,et al.  Fuel Properties of Highly Polyunsaturated Fatty Acid Methyl Esters. Prediction of Fuel Properties of Algal Biodiesel , 2012 .

[19]  J. R. Benemann,et al.  Utilization of carbon dioxide from fossil fuel-burning power plants with biological systems , 1993 .

[20]  B. Rittmann,et al.  Disruption of Synechocystis PCC 6803 for lipid extraction. , 2012, Water science and technology : a journal of the International Association on Water Pollution Research.

[21]  D. Chapman.  Phase transitions and fluidity characteristics of lipids and cell membranes , 1975, Quarterly Reviews of Biophysics.

[22]  Kouji Matsumoto,et al.  Role of Slr1045 in environmental stress tolerance and lipid transport in the cyanobacterium Synechocystis sp. PCC6803. , 2012, Biochimica et biophysica acta.

[23]  Bruce E Rittmann,et al.  Nutrient acquisition and limitation for the photoautotrophic growth of Synechocystis sp. PCC6803 as a renewable biomass source , 2011, Biotechnology and bioengineering.

[24]  Xuefeng Lu,et al.  A perspective: photosynthetic production of fatty acid-based biofuels in genetically engineered cyanobacteria. , 2010, Biotechnology advances.

[25]  Y. Kanesaki,et al.  Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. , 2002, Biochemical and biophysical research communications.

[26]  B. Rittmann,et al.  Effects of temperature shifts on growth rate and lipid characteristics of Synechocystis sp. PCC6803 in a bench-top photobioreactor. , 2011, Bioresource technology.

[27]  S. Atsumi,et al.  Cyanobacterial biofuel production. , 2012, Journal of biotechnology.

[28]  Yebo Li,et al.  Comparison of Synechocystis sp. PCC6803 and Nannochloropsis salina for lipid production using artificial seawater and nutrients from anaerobic digestion effluent. , 2013, Bioresource technology.

[29]  R. Prasanna,et al.  New insights into the biodiversity and applications of cyanobacteria (blue-green algae)—Prospects and challenges , 2013 .

[30]  B. Rittmann.  Opportunities for renewable bioenergy using microorganisms. , 2008, Biotechnology and bioengineering.

[31]  Qiang Hu,et al.  Handbook of microalgal culture , 2003 .

[32]  A. Grossman,et al.  The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. , 2001, The Journal of biological chemistry.

[33]  N. Murata,et al.  Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. , 1995, The Biochemical journal.

[34]  G. Price,et al.  Temperature modulation of fatty acid profiles for biofuel production in nitrogen deprived Chlamydomonas reinhardtii. , 2013, Bioresource technology.

[35]  Bruce E. Rittmann,et al.  Photosynthetic bioenergy utilizing CO2: an approach on flue gases utilization for third generation biofuels , 2015 .

[36]  R. Sinha,et al.  Role of Lipids and Fatty Acids in Stress Tolerance in Cyanobacteria , 2002 .

[37]  L. Sherman,et al.  Environmental pH affects photoautotrophic growth of Synechocystis sp. PCC 6803 strains carrying mutations in the lumenal proteins of PSII. , 2013, Plant & cell physiology.

[38]  Bruce E Rittmann,et al.  Evaluation of methods to extract and quantify lipids from Synechocystis PCC 6803. , 2011, Bioresource technology.

[39]  D. Los,et al.  Structure and expression of fatty acid desaturases. , 1998, Biochimica et biophysica acta.

[40]  Peter Delves,et al.  Encyclopedia of life sciences , 2009 .

[41]  P. Webley,et al.  Extraction of oil from microalgae for biodiesel production: A review. , 2012, Biotechnology advances.

[42]  N. Murata,et al.  Unsaturation of fatty acids in membrane lipids enhances tolerance of the cyanobacterium Synechocystis PCC6803 to low-temperature photoinhibition. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Robert Verpoorte,et al.  Renewable energy from Cyanobacteria: energy production optimization by metabolic pathway engineering , 2011, Applied Microbiology and Biotechnology.

[44]  Philip Owende,et al.  Biofuels from microalgae—A review of technologies for production, processing, and extractions of biofuels and co-products , 2010 .