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Salinity-induced oxidative stress-mediated change in fatty acids composition of cyanobacterium Synechococcus sp. PCC7942

  • E. Verma
  • S. Singh
  • Niveshika
  • A. K. MishraEmail author
Original Paper
  • 49 Downloads

Abstract

The present study was undertaken to examine the salinity stress-induced physiological and biochemical alterations in the cyanobacterium Synechococcus sp. PCC 7942. Cyanobacterial cultures supplemented with different concentrations of NaCl were evaluated for growth, carbohydrate, total lipid, ROS generation, and stress biomarkers to evaluate the ROS-mediated lipid production in Synechococcus 7942. Salt concentration of 500 mM induced a five- and threefold increase in the production of carbohydrates and lipids, respectively. The fatty acids composition in terms of total quantity and oleic acid content of the investigated species was also improved as the salinity level increased from 0 to 500 mM NaCl. The data showed maximum MUFA production at 10 mM NaCl with dominance of palmitoleic acid (88.3%) and oleic acid (0.31%), whereas PUFA was found to be maximally produced at 250 mM NaCl with dominance of linoleic acid. Salt stress enhanced the accumulation of carbohydrate and total lipids and antioxidative enzymes, and modulates the fatty acids and hydrocarbon composition of cyanobacterium. Production of fatty acid and hydrocarbon under saline conditions indicates that salinity can be used as a factor to modulate the biochemical pathways of cyanobacteria toward efficient biofuel production.

Keywords

Biofuel FAMEs Lipids Hydrocarbons Salinity Synechococcus sp. PCC 7942 

Abbreviations

APX

Ascorbate peroxidase

CAT

Catalase

CH

Cyclic hydrocarbon

FAMEs

Fatty acid methyl esters

GC/MS

Gas chromatography/mass spectrometry

MDA

Malondialdehyde

MUFA

Monounsaturated fatty acid

PUFA

Polyunsaturated fatty acid

ROS

Reactive oxygen species

SFA

Saturated fatty acid

SH

Saturated hydrocarbon

SOD

Superoxide dismutase

USH

Unsaturated hydrocarbon

Notes

Acknowledgements

We are thankful to the Head, Department of Botany, Banaras Hindu University, Varanasi, India, for providing laboratory facilities. We thank Prof. Karl Forchhammer, Department of Organismic Interactions (Microbiology), Interfaculty Institute of Microbiology and Infection, Auf der Morgenstelle, 2872076, University of Tübingen, Germany, for providing Synechococcus sp. PCC 7942 strain. Two of us (Ekta Verma and Niveshika) are thankful to the UGC, New Delhi, for financial support in the form of JRF.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13762_2018_1720_MOESM1_ESM.tif (643 kb)
Fig. S1. Growth of the cyanobacterium Synechococcus sp. in terms of dry weight (TIFF 642 kb)
13762_2018_1720_MOESM2_ESM.tif (625 kb)
Figure S2 DCF fluorescence-based G/R ratio of Synechococcus sp. obtained from fluorescence microscopic analysis under NaCl stress (TIFF 625 kb)
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Figure S3. GC/MS Chromatograms of control, 10, 50, 100, 250 and 500 mM NaCl-treated cyanobacterial cells (Fig. 1a, 1b, 1c, 1d, 1e, 1f, respectively) (EPS 3134 kb)
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Supplementary material 4 (EPS 3137 kb)
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Supplementary material 5 (EPS 3135 kb)
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Supplementary material 6 (EPS 3130 kb)
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Supplementary material 7 (EPS 3130 kb)
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Supplementary material 8 (EPS 3133 kb)
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Supplementary material 9 (DOCX 663 kb)
13762_2018_1720_MOESM10_ESM.docx (580 kb)
Supplementary material 10 (DOCX 580 kb)

References

  1. Ali S, Huang Z, Li H, Bashir MH, Ren S (2013) Antioxidant enzyme influences germination, stress tolerance, and virulence of Isaria fumosorosea. J Basic Microbiol 53:489–497CrossRefGoogle Scholar
  2. Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I, Murata N (2001) Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol 125:1842–1853CrossRefGoogle Scholar
  3. Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol 130:1443–1453CrossRefGoogle Scholar
  4. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341CrossRefGoogle Scholar
  5. Bates LS, Waldren RP, Tear ID (1975) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  6. Becker EW (1994) Microalgae biotechnology and microbiology. Cambridge University Press, Great BritainGoogle Scholar
  7. Bhaduri AM, Fulekar MH (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sci Biotechnol 11:55–69CrossRefGoogle Scholar
  8. Chance B, Maehly AC (1995) Assay of catalase and peroxidases. Methods Enzymol 2:764–775CrossRefGoogle Scholar
  9. Chokshi K, Pancha I, Trivedi K, George B, Maurya R, Ghosh A, Mishra S (2015) Biofuel potential of the newly isolated microalgae Acutodesmus dimorphus under temperature induced oxidative stress conditions. Bioresour Technol 180:161–171CrossRefGoogle Scholar
  10. de Farias Silva CE, Bertucco A (2016) Bioethanol from microalgae and cyanobacteria: a review and technological outlook. Process Biochem.  https://doi.org/10.1016/j.procbio.2016.02.016 Google Scholar
  11. del Rio LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335CrossRefGoogle Scholar
  12. DuBois M, Gilles K, Hamilton J, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  13. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509Google Scholar
  14. Giannopolitis CN, Ries SK (1977) Superoxide dismutase, I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  15. Gill PK, Sharma AD, Singh P, Bhullar SS (2002) Osmotic stress induced changes in germination, growth and soluble sugar contents of Sorghum bicolor (L.) Moench seeds under various abiotic stresses. Plant Physiol 128:12–25Google Scholar
  16. Gomaa MA, Al-Haj L, Abed RMM (2016) Metabolic engineering of Cyanobacteria and microalgae for enhanced production of biofuels and high-value products. J Appl Microbiol 121:919–931CrossRefGoogle Scholar
  17. Greenwell HC, Laurens LM, Shields RJ, Lovitt RW, Flynn KJ (2010) Placing microalgae on the biofuels priority list: a review of the technological challenges. J R Soc Interface 7:703–726CrossRefGoogle Scholar
  18. He YY, Hader DP (2002) UV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N acetyl cysteine. J Photochem Photobiol 66:115–124CrossRefGoogle Scholar
  19. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  20. Heidorn T, Camsund D, Huang HH, Lindberg P, Oliveira P, Stensjo K, Lindblad P (2011) Synthetic biology in cyanobacteria engineering and analyzing novel functions. Methods Enzymol 497:539–579CrossRefGoogle Scholar
  21. Huang HH, Camsund D, Lindblad P, Heidorn T (2010) Design and characterization of molecular tools for a synthetic biology approach towards developing cyanobacterial biotechnology. Nucleic Acids Res 38:2577–2593CrossRefGoogle Scholar
  22. Jaffel K, Sai S, Bouraoui NK, Ammar RB, Legendre L, Lachaal M, Marzouk B (2011) Influence of salt stress on growth, lipid peroxidation and antioxidative enzyme activity in borage (Borago officinalis L.). Plant Biosyst 145:362–369CrossRefGoogle Scholar
  23. Kang JX, Wang J (2005) A simplified method for analysis of polyunsaturated fatty acids. BMC Biochem 6:5CrossRefGoogle Scholar
  24. Kiran B, Pathak K, Kumar R, Deshmukh D, Rani N (2016) Influence of varying nitrogen levels on lipid accumulation in Chlorella sp. Int J Environ Sci Technol 13:1823–1832CrossRefGoogle Scholar
  25. Kirroliaa A, Bishnoia NR, Singh N (2011) Salinity as a factor affecting the physiological and biochemical traits of Scenedesmus quadricauda. J Algal Biomass Utln 2:28–34Google Scholar
  26. Koksharova OA, Wolk CP (2002) Genetic tools for cyanobacteria. Appl Microbiol Biotechnol 58:123–137CrossRefGoogle Scholar
  27. Lu C, Zhang J (2000) Role of light in the response of PSII photochemistry to salt stress in the cyanobacterium Spirulina platensis. J Exp Bot 51:911–917CrossRefGoogle Scholar
  28. Ludwig M, Bryant DA (2012) Synechococcus sp. strain PCC 7002 transcriptome: acclimation to temperature, salinity, oxidative stress, and mixotrophic growth conditions. Front Microbiol 3:354Google Scholar
  29. Machado IMP, Atsumi S (2012) Cyanobacterial biofuel production. J Biotechnol 162:50–56CrossRefGoogle Scholar
  30. Mackinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322Google Scholar
  31. Martínez-Roldán AJ, Perales-Vela HV, Cañizares-Villanueva RO, Torzillo G (2014) Physiological response of Nannochloropsis sp. to saline stress in laboratory batch cultures. J Appl Phycol 26:115–121CrossRefGoogle Scholar
  32. Meury J (1988) Glycine-betaine reverses the effects of osmotic stress on DNA replication and cellular division in Escherichia coli. Arch Microbiol 149:232–239CrossRefGoogle Scholar
  33. Monshupanee T, Incharoensakdi A (2013) Enhanced accumulation of glycogen, lipids and polyhydroxybutyrate under optimal nutrients and light intensities in the cyanobacterium Synechocystis sp. PCC 6803. J Appl Microbiol 116:830–838CrossRefGoogle Scholar
  34. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  35. Osundeko O, Davies H, Pittman JK (2013) Oxidative stress-tolerant microalgae strains are highly efficient for biofuel feedstock production on wastewater. Biomass Bioenergy 56:284–294CrossRefGoogle Scholar
  36. Pal D, Khozin-Goldberg I, Cohen Z, Boussiba S (2011) The effect of light, salinity, and nitrogen availability on lipid production by Nannochloropsis sp. Appl Microbiol Biotechnol 90:1429–1441CrossRefGoogle Scholar
  37. Pancha I, Chokshi K, George B, Ghosh T, Paliwal C, Maurya R, Mishra S (2014) Nitrogen stress triggered biochemical and morphological changes in the microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 156:146–154CrossRefGoogle Scholar
  38. Pancha I, Chokshi K, Maurya RK, Trivedi K, Patidar SK, Ghosh A, Mishra S (2015) Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 189:341–348CrossRefGoogle Scholar
  39. Peralta-Yahya PP, Keasling JD (2010) Advanced biofuel production in microbes. J Biotechnol 5:147–162CrossRefGoogle Scholar
  40. Piuri M, Sanchez-Rivas C, Ruzal SM (2005) Cell wall modifications during osmotic stress in Lactobacillus casei. J Appl Microbiol 98:84–95CrossRefGoogle Scholar
  41. Quintana N, Van der Kooy F, Van de Rhee MD, Voshol GP, Verpoorte R (2011) Renewable energy from Cyanobacteria: energy production optimization by metabolic pathway engineering. Appl Microbiol Biotechnol 91:471–490CrossRefGoogle Scholar
  42. Rittmann BE (2008) Opportunities for renewable bioenergy using microorganisms. Biotechnol Bioeng 100:203–212CrossRefGoogle Scholar
  43. Ruffing AM (2011) Engineered cyanobacteria: teaching an old bug new tricks. Bioeng Bugs 2:136–149CrossRefGoogle Scholar
  44. Salama ES, Kim HC, Abou-Shanab RAI, Ji MK, Oh YK, Kim SH, Jeon BH (2013) Biomass, lipid content, and fatty acid composition of freshwater Chlamydomonas mexicana and Scenedesmus obliquus grown under salt stress. Bioprocess Biosyst Eng 36:827–833CrossRefGoogle Scholar
  45. Scharlemann JP, Laurance WF (2008) Environmental science. How green are biofuels? Science 319:43–44CrossRefGoogle Scholar
  46. Song D, Fu J, Shi D (2008) Exploitation of oil-bearing microalgae for biodiesel. Chin J Biotechnol 24:341–348CrossRefGoogle Scholar
  47. Suutari M, Laakso S (1992) Microbial fatty acids and thermal adaptation. Crit Rev Microbiol 20:285–328CrossRefGoogle Scholar
  48. Takagi M, Karseno Yoshida T (2006) Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J Biosci Bioeng 101:223–226CrossRefGoogle Scholar
  49. Warr SRC, Reed RH, Chudek JA, Foster R, Stewart WDP (1985) Osmotic adjustment in Spirulina platensis. Planta 163:424–429CrossRefGoogle Scholar
  50. Yilancioglu K, Cokol M, Pastirmaci I, Erman B, Cetiner S (2014) Oxidative stress is a mediator for increased lipid accumulation in a newly isolated Dunaliella salina strain. PLoS ONE 9:e91957CrossRefGoogle Scholar
  51. Zhu L, Zhang X, Ji L, Song X, Kuang C (2007) Changes of lipid content and fatty acid composition of Schizochytrium limacinum in response to different temperatures and salinities. Process Biochem 42:210–214CrossRefGoogle Scholar

Copyright information

© Islamic Azad University (IAU) 2018

Authors and Affiliations

  1. 1.Laboratory of Microbial Genetics, Department of BotanyBanaras Hindu UniversityVaranasiIndia

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