Skip to main content
SpringerLink
Log in

Screening for polar lipids, antioxidant, and anti-inflammatory activities of Gloeothece sp. lipid extracts pursuing new phytochemicals from cyanobacteria

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Cyanobacteria are photosynthetic organisms that produce a variety of molecules with beneficial properties for applications in fields such as food and feed, pharmaceuticals, and industrial chemicals. In particular, polar lipids from algae are gaining interest because they have been associated with bioactive properties and health benefits. Cyanobacteria have been little studied, particularly in the case of Gloeothece sp. whose polar lipidome is unknown. We have used a high-resolution liquid chromatography mass spectrometry-based approach to identify the polar lipidome of Gloeothece sp. and have also evaluated their antioxidant and anti-inflammatory potential. Results obtained allowed the identification of 162 lipid molecular species from glycolipids, betaine lipids, and phospholipid categories. These molecular species were esterified to fatty acids (FA) with C16 and C18 chain length and with a degree of unsaturation (DoU) ranging between 0 and 4. Some of the lipid species identified in the lipidome are recognized for their bioactive properties. Therefore, the antioxidant capacity of the polar lipid extracts was evaluated against superoxide (O2·−) and nitric oxide (·NO) radicals and the anti-inflammatory capacity using the COX-2 Enzyme Activity Assay Kit. The lipid extracts displayed antioxidant capacity toward O2·− and ·NO radicals in a dose-dependent manner with IC50 of 939.8 ± 15.6 and 1033.7 ± 17.9 μg mL−1, respectively. The extracts showed anti-inflammatory activity by the inhibition of the conversion of arachidonic acid to prostaglandin H2 (PGH2) via inhibition of COX-2, with the lowest concentration tested of 10 μg mL−1 inhibiting the production of PGH2 by about 58%. Overall, these results suggest that the extracts from Gloeothece could be a source of natural product, fostering increasing interest of cyanobacterial exploitation to produce food and metabolites with potential bioactive properties useful for nutraceutical, cosmetics, and medicinal applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amaro HM, Guedes AC, Malcata FX (2011) Science against microbial pathogens: communicating current research and technological advances. In: Mendez-Vilas A (ed) Antimicrobial activities of microalgae: an invited review. Formatex, New York, pp 1272–1280

    Google Scholar 

  • Amaro HM, Fernandes F, Valentão P, Andrade PB, Sousa-Pinto I, Malcata FX, Guedes AC (2015) Effect of solvent system on extractability of lipidic components of Scenedesmus obliquus (M2-1) and Gloeothece sp. on antioxidant scavenging capacity thereof. Mar Drugs 13:6453–6471

    CAS  PubMed  PubMed Central  Google Scholar 

  • Amaro HM, Catarina Guedes A, Preto MAC, Sousa-Pinto I, Malcata FX (2018) Gloeothece sp. as a nutraceutical source-an improved method of extraction of carotenoids and fatty acids. Mar Drugs 16:327

    PubMed Central  Google Scholar 

  • Antonelli M, Benedetti B, Cavaliere C, Cerrato A, La Barbera G, Montone CM, Piovesana S, Laganà A (2019) Enrichment procedure based on graphitized carbon black and liquid chromatography-high resolution mass spectrometry for elucidating sulfolipids composition of microalgae. Talanta 205:120162

    CAS  PubMed  Google Scholar 

  • Antonopoulou S, Oikonomou A, Karantonis HC, Fargopoulou E, Pantazidou A (2002) Isolation and structural elucidation of biologically active phospholipids from Scytonema julianum (cyanobacteria). Biochem J 293:287–293

    Google Scholar 

  • Aued-Pimentel S, Lago JHG, Chaves MH, Kumagai EE (2004) Evaluation of a methylation procedure to determine cyclopropenoids fatty acids from Sterculia striata St. Hil Et Nauds seed oil. J Chromatogr A 1054:235–239

    CAS  PubMed  Google Scholar 

  • Banskota AH, Gallant P, Stefanova R, Melanson R, O’Leary SJB (2013a) Monogalactosyldiacylglycerols, potent nitric oxide inhibitors from the marine microalga Tetraselmis chui. Nat Prod Res 27:1084–1090

    CAS  PubMed  Google Scholar 

  • Banskota AH, Stefanova R, Sperker S, McGinn PJ (2013b) New diacylglyceryltrimethylhomoserines from the marine microalga Nannochloropsis granulata and their nitric oxide inhibitory activity. J Appl Phycol 25:1513–1521

    CAS  Google Scholar 

  • Banskota AH, Stefanova R, Sperker S, Lall SP, Craigie JS, Hafting JT, Critchley AT (2014) Polar lipids from the marine macroalga Palmaria palmata inhibit lipopolysaccharide-induced nitric oxide production in RAW264.7 macrophage cells. Phytochemistry 101:101–108

    CAS  PubMed  Google Scholar 

  • Barkia I, Saari N, Manning SR (2019) Microalgae for high-value products towards human health and nutrition. Mar Drugs 17:1–29

    Google Scholar 

  • Becker EW (1994) Microalgae: biotechnology and microbiology. Cambridge University Press, New York, pp 177–181

    Google Scholar 

  • Benning C, Huang ZH, Gage DA (1995) Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation. Arch Biochem Biophys 317:103–111

    CAS  PubMed  Google Scholar 

  • Bergé JP, Debiton E, Dumay J, Durand P, Barthomeuf C (2002) In vitro anti-inflammatory and anti-proliferative activity of sulfolipids from the red alga Porphyridium cruentum. J Agric Food Chem 50:6227–6232

    PubMed  Google Scholar 

  • Boudière L, Michaud M, Petroutsos D, Rébeillé F, Falconet D, Bastien O, Roy S, Finazzi G, Rolland N, Jouhet J, Block AB, Maréchal E (2014) Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim Biophys Acta Bioenerg 1837:470–480

    Google Scholar 

  • Bruno A, Rossi C, Marcolongo G, Di Lena A, Venzo A, Berrie CP, Corda D (2005) Selective in vivo anti-inflammatory action of the galactolipid monogalactosyldiacylglycerol. Eur J Pharmacol 524:159–168

    CAS  PubMed  Google Scholar 

  • Caudales R, Wells JM (1992) Differentiation of free-living Anabaena and Nostoc cyanobacteria on the basis of fatty acid composition. Int J Syst Bacteriol 42:246–251

    CAS  PubMed  Google Scholar 

  • Caudales R, Wells JM, Butterfield JE (2000) Cellular fatty acid composition of cyanobacteria assigned to subsection II, order Pleurocapsales the cellular fatty acid composition of five of the six genera of unicellular reported for the unicellular cyanobacteria of subsection I, order Chroococcales. Int J Syst Evol Microbiol 3:1029–1034

    Google Scholar 

  • Cohen Z, Margheri MC, Tomaselli L (1995) Chemotaxonomy of cyanobacteria. Phytochem 40:1155–1158

    CAS  Google Scholar 

  • da Costa E, Melo T, Moreira ASP, Alves E, Domingues P, Calado R, Abreu MH, Domingues MR (2015) Decoding bioactive polar lipid profile of the macroalgae Codium tomentosum from a sustainable IMTA system using a lipidomic approach. Algal Res 12:388–397

    Google Scholar 

  • da Costa E, Silva J, Mendonça SHS, Abreu MH, Domingues MR (2016) Lipidomic approaches towards deciphering glycolipids from microalgae as a reservoir of bioactive lipids. Mar Drugs 14:1–27

    Google Scholar 

  • da Costa E, Azevedo V, Melo T, Rego AM, Evtuguin DV, Domingues P, Calado R, Pereira R, Abreu MH, Domingues MR (2018) High-resolution lipidomics of the early life stages of the red seaweed Porphyra dioica. Molecules 23:1–20

    Google Scholar 

  • da Costa E, Domingues P, Melo T, Coelho E, Pereira R, Calado R, Abreu MH, Domingues MR (2019) Lipidomic signatures reveal seasonal shifts on the relative abundance of high-valued lipids from the brown algae Fucus vesiculosus. Mar Drugs 17:1–23

    CAS  Google Scholar 

  • Deviram G, Mathimani T, Anto S, Ahamed TS, Ananthd DA, Pugazhendhie A (2020) Applications of microalgal and cyanobacterial biomass on a way to safe, cleaner and a sustainable environment. J Clean Prod 253:3–21

    Google Scholar 

  • Granafei S, Losito I, Palmisano F, Cataldi TRI (2017) Unambiguous regiochemical assignment of sulfoquinovosyl mono- and diacylglycerols in parsley and spinach leaves by liquid chromatography/electrospray ionization sequential mass spectrometry assisted by regioselective enzymatic hydrolysis. Rapid Commun Mass Spectrom 31:1499–1509

    CAS  PubMed  Google Scholar 

  • Guedes AC, Amaro HM, Barbosa CR, Pereira RD, Malcata FX (2011) Fatty acid composition of several wild microalgae and cyanobacteria, with a focus on eicosapentaenoic, docosahexaenoic and α-linolenic acids for eventual dietary uses. Food Res Int 44:2721–2729

    CAS  Google Scholar 

  • Guedes AC, Amaro HM, Sousa-Pinto I, Malcata FX (2019) Chapter 16 - algal spent biomass – a pool of applications. In: Pandey A, Chang J-S, Soccol CR, Lee D-J, Chisti Y (eds) Biofuels from algae: biomass, biofuels, Biochemicals, 2nd edn. Elsevier, San Diego, pp 397–433

    Google Scholar 

  • Hadad N, Levy R (2012) The synergistic anti-inflammatory effects of lycopene, lutein, β-carotene, and carnosic acid combinations via redox-based inhibition of NF-κB signaling. Free Radic Biol Med 53:1381–1389

    CAS  PubMed  Google Scholar 

  • Han X (2016) Lipidomics: comprehensive mass spectrometry of lipids. John Wiley & Sons, New York

    Google Scholar 

  • Jensen GS (2001) Blue-green algae as an immuno-enhancer and biomodulator. Jana 3:24–30

    Google Scholar 

  • Kalsum U, Kusuma HS, Roesyadi A, Mahfud M (2019) Lipid extraction from Spirulina platensis using microwave for biodiesel production. Korean Chem Eng Res 57:301–304

    CAS  Google Scholar 

  • Kebede M, Admassu S (2019) Application of antioxidants in food processing industry: options to improve the extraction yields and market value of natural products. Adv Food Technol Nutr Sci – Open J 5:38–49

    CAS  Google Scholar 

  • Khan MI, Shin JH, Kim JD (2018) The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb Cell Factories 17:1–21

    Google Scholar 

  • Kim YH, Choi J-S, Yoo JS, Park YM, Kim MS (1999) Structural Identification of glycerolipid molecular species isolated from cyanobacterium Synechocystis sp . PCC 6803 using fast atom bombardment tandem mass spectrometry. Anal Biochem 267:260–270

    CAS  PubMed  Google Scholar 

  • Kumar R, Biswas K, Singh PK, Elumalai S, Shukla P, Pabbi S (2017) Lipid production and molecular dynamics simulation for regulation of accD gene in cyanobacteria under different N and P regimes. Biotechnol Biofuels 10:1–14

    Google Scholar 

  • La Barbera G, Antonelli M, Cavaliere C, Cruciani G, Goracci L, Montone CM, Piovesana S, Laganà A, Capriotti AL (2018) Delving into the polar lipidome by optimized chromatographic separation, high-resolution mass spectrometry, and comprehensive identification with Lipostar: microalgae as case study. Anal Chem 90:12230–12238

    PubMed  Google Scholar 

  • Lee JL, Mukhtar H, Bickers DR, Kopelovich L, Athar M (2013) Cyclooxygenases in the skin: pharmacological and toxicological implications. Toxicol Appl Pharmacol 192:294–306

    Google Scholar 

  • Melo T, Alves E, Azevedo V, Martins AS, Neves B, Domingues P, Calado R, Abreu MH, Domingues MR (2015) Lipidomics as a new approach for the bioprospecting of marine macroalgae — unraveling the polar lipid and fatty acid composition of Chondrus crispus. Algal Res 8:181–191

    Google Scholar 

  • Montero O (2011) Lipid profiling of Synechococcus sp . PCC7002 and two related strains by HPLC coupled to ESI- (Ion Trap) -MS / MS. Z Naturforsch C 66:149–158

    CAS  PubMed  Google Scholar 

  • Mukherjee B, Ghosh MK, Hossain CM (2011) Anticancer potential of vitamin A and betacarotene: mechanistic approach. NSHM J Pharm Healthcare Manage 2:1–12

  • Mundt S, Kreitlow S, Jansen R (2003) Fatty acids with antibacterial activity from the cyanobacterium Oscillatoria redekei HUB 051. J Appl Phycol 15:263–267

    CAS  Google Scholar 

  • Murata N, Nishida I (1987) Lipids of blue-green algae (cyanobacteria). Lipids Struct Funct 9:315–347

    CAS  Google Scholar 

  • Murphy RC (2015) Tandem mass spectrometry of lipids. New developments in Mass spectrometry No.4., Royal Society of Chemistry,

  • Plohnke N, Seidel T, Kahmann U, Rögner M, Schneider D, Rexroth S (2015) The proteome and lipidome of Synechocystis sp. PCC 6803 cells grown under light-activated heterotrophic conditions. Mol Cell Proteomics 14:572–584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Plouguerné E, da Gama BAP, Pereira RC, Barreto-Bergter E (2014) Glycolipids from seaweeds and their potential biotechnological applications. Front Cell Infect Microbiol 4:1–3

    Google Scholar 

  • Reshef V, Mizrachi E, Maretzki T, Silberstein C, Loya S, Hizi A, Carmeli S (1997) New acylated sulfoglycolipids and digalactolipids and related known glycolipids from cyanobacteria with a potential to inhibit the reverse transcriptase of HIV-1. J Nat Prod 60:1251–1260

    CAS  PubMed  Google Scholar 

  • Řezanka T, Víden I, Go JV, Dor I, Dembitsky VM (2003) Polar lipids and fatty acids of three wild cyanobacterial strains of the genus Chroococcidiopsis. Folia Microbiol (Praha) 48:781–786

    Google Scholar 

  • Sakurai I, Shen JR, Leng J, Ohashi S, Kobayashi M, Wada H (2006) Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. J Biochem 140:201–209

    CAS  PubMed  Google Scholar 

  • Sallal AK, Nimer NA, Radwan SS (1990) Lipid and fatty acid composition of freshwater cyanobacteria. J Gen Microbiol 136:2043–2048

    CAS  Google Scholar 

  • Schymanski EL, Jeon J, Gulde R, Fenner K, Ruff M, Singer HP, Hollender J (2014) Identifying small molecules via high resolution mass spectrometry: communicating confidence. Environ Sci Technol 48:2097–2098

    CAS  PubMed  Google Scholar 

  • Sharathchandra K, Rajashekhar M (2011) Total lipid and fatty acid composition in some freshwater cyanobacteria. J Algal Biomass Utln 2:83–97

    Google Scholar 

  • Sidhu KS (2003) Health benefits and potential risks related to consumption of fish or fish oil. Regul Toxicol Pharmacol 38:336–344

    CAS  PubMed  Google Scholar 

  • Simopoulos AP (1999) Essential fatty acids in health and chronic disease. Am J Clin Nutr 70:560S–569S

    CAS  PubMed  Google Scholar 

  • Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 233:674–688

    CAS  Google Scholar 

  • Singh S, Kate BN, Banecjee UC (2005) Bioactive compounds from cyanobacteria and microalgae: an overview. Crit Rev Biotechnol 25:73–95

    CAS  PubMed  Google Scholar 

  • Singh JS, Kumar A, Rai AN, Singh DP (2016) Cyanobacteria: a precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 7:1–19

    CAS  Google Scholar 

  • Singh R, Parihar P, Singh M, Bajguz A, Kumar J, Singh S, Singh VP, Prasad SM (2017) Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Front Microbiol 8:1–37

    Google Scholar 

  • Sohlenkamp C, Geiger O (2015) Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev 40:133–159

    PubMed  Google Scholar 

  • Terme N, Boulho R, Kucma JP, Bourgougnon N, Bedoux G (2018) Radical scavenging activity of lipids from seaweeds isolated by solid-liquid extraction aand supercritical fluids. OCL 25:D505

    Google Scholar 

  • Van Eerden FJ, De Jong DH, De Vries AH, Wassenaar T, Marrink SJ (2015) Characterization of thylakoid lipid membranes from cyanobacteria and higher plants by molecular dynamics simulations. Biochim Biophys Acta Biomembr 1848:1319–1330

    Google Scholar 

Download references

Funding

The FCT/MCTES (Portugal) provided the financial support to CESAM (UIDB/50017/2020+UIDP/50017/2020), QOPNA ((FCT UID/QUI/00062/2019) and LAQV/REQUIMTE (UIDB/50006/2020), CIIMAR (UIDB/04423/2020 and UIDP/04423/2020), and RNEM (LISBOA-01-0145-FEDER-402-022125), through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. Elisabete da Costa (BPD/UI51/5042/2018) received grant within framework of the project GENIALG—Genetic diversity exploitation for innovative macro-alga biorefinery (ANR-15-MRSE-0015) funded by European Union’s Horizon 2020 Framework Programme. Tânia Melo research contract is funded under the project OMICS 4ALGAE: Lipidomic tools for chemical phenotyping, traceability and valorisation of seaweeds from aquaculture as a sustainable source of high added value compounds (POCI-01-0145-FEDER-030962), funded by Centro2020, through FEDER and PT2020. This is a Marine Lipidomics Laboratory & CIIMAR contribution. This work was supported by the projects ZEBRALGRE (PTDC/CVT-WEL/5207/2014) project, funded by FEDER, through COMPETE2020-Programa Operacional Competitividade e Internacionalização (POCI), and by national funds (OE), through FCT/MCTES.

Author information

Authors and Affiliations

  1. CESAM – Centre for Environmental and Marine Studies, Department of Chemistry, University of Aveiro, Santiago University Campus, 3810-193, Aveiro, Portugal

    Elisabete da Costa, Tânia Melo & M. Rosário Domingues

  2. Mass Spectrometry Centre, LAQV-REQUIMTE, Department of Chemistry, University of Aveiro, Santiago University Campus, 3810-193, Aveiro, Portugal

    Elisabete da Costa, Tânia Melo & M. Rosário Domingues

  3. CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Novo Edifício do Terminal de Cruzeiros de Leixões, Avenida General Norton de Matos, s/n, 4450-208, Matosinhos, Portugal

    Helena M. Amaro & A. Catarina Guedes

Authors
  1. Elisabete da Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Helena M. Amaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tânia Melo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Catarina Guedes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Rosário Domingues
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elisabete da Costa.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOC 560 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Costa, E., Amaro, H.M., Melo, T. et al. Screening for polar lipids, antioxidant, and anti-inflammatory activities of Gloeothece sp. lipid extracts pursuing new phytochemicals from cyanobacteria. J Appl Phycol 32, 3015–3030 (2020). https://doi.org/10.1007/s10811-020-02173-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02173-6

Keywords

Search

Navigation