Freshwater algae Cladophora glomerata and Vaucheria sp. from Serbia as sources of bioactive compounds: chemical analysis and biological activities

Authors

  • Olgica D. Stefanović University of Kragujevac, Faculty of Science, Department of Biology and Ecology, Radoja Domanovića 12, 34 000 Kragujevac, Serbia https://orcid.org/0000-0003-1255-7706
  • Aleksandra B. Rakonjac 1. University of Kragujevac, Faculty of Science, Department of Biology and Ecology, Radoja Domanovića 12, 34 000 Kragujevac, Serbia; 2. Institute for Vegetable Crops, Karađorđeva 71, 11 420 Smederevska Palanka, Serbia https://orcid.org/0000-0002-7347-4296
  • Danijela D. Nikodijević University of Kragujevac, Faculty of Science, Department of Biology and Ecology, Radoja Domanovića 12, 34 000 Kragujevac, Serbia https://orcid.org/0000-0002-6453-0313
  • Sara D. Milojević University of Kragujevac, Faculty of Science, Department of Biology and Ecology, Radoja Domanovića 12, 34 000 Kragujevac, Serbia
  • Anica Dinić University of Kragujevac, Faculty of Science, Department of Biology and Ecology, Radoja Domanovića 12, 34 000 Kragujevac, Serbia
  • Snežana B. Simić University of Kragujevac, Faculty of Science, Department of Biology and Ecology, Radoja Domanovića 12, 34 000 Kragujevac, Serbia https://orcid.org/0000-0003-3273-2858

DOI:

https://doi.org/10.2298/ABS240215012S

Keywords:

antioxidant activity, antimicrobial activity, antibiofilm activity, cytotoxicity, freshwater algae, algal extracts

Abstract

Paper description:

  • There is growing interest in novel sources of biologically active compounds, including freshwater macroalgae whose bioactivities are largely unexplored.
  • Ethanol and acetone extracts of Cladophora glomerata and Vaucheria were prepared.
  • Total phenolic and pigment contents were determined. In vitro bioactivities, including antioxidant potential, antimicrobial, antibiofilm activities, and cytotoxicity were examined.
  • glomerata and Vaucheria sp. extracts are a valuable source of bioactive compounds.

Abstract: We examined potential biological activities of two taxa of freshwater algae, Cladophora glomerata and Vaucheria sp., from Serbia. The total phenolic and pigment contents, antioxidant potential, antimicrobial, antibiofilm activities, and cytotoxicity of the ethanol and acetone extracts were evaluated. The extracts were also subjected to Fourier transform infrared spectroscopy (FTIR) analysis. The levels of total phenolic compounds, chlorophylls a and b, and carotenoids varied based on both the algal taxa and the type of extracts. FTIR analysis showed the presence of lipids, unsaturated fatty acids, protein, carbohydrates, and phenols in the algal extracts. The extracts had moderate DPPH radical scavenging activity and lower reducing power compared with ascorbic acid. The antimicrobial activity expressed as minimum inhibitory concentrations ranged from 0.31 mg/mL to 10 mg/mL. The strains of Staphylococcus aureus and Bacillus cereus isolated from food samples, as well as S. aureus ATCC 25923, were the most sensitive. For the first time, the antibiofilm activity test revealed 98.7% inhibition of S. aureus biofilm formation. The extracts exhibited cytotoxic effects on choriocarcinoma JAR cells but without selectivity on normal fetal lung fibroblast MRC-5 cells. This is the first report on the biological activities of freshwater macroalgae from Serbia.

Downloads

Download data is not yet available.

References

Barsanti L, Gualtieri P. Algae: anatomy, biochemistry, and biotechnology. 2nd ed. Boca Raton: CRC press; 2006. 301 p.

Silva A, Silva SA, Lourenço-Lopes C, Jimenez-Lopez C, Carpena M, Gullón P, Fraga-Corral M, Domingues VF, Barroso MF, Simal-Gandara J, Prieto MA. Antibacterial Use of Macroalgae Compounds against Foodborne Pathogens. Antibiotics (Basel). 2020;9(10):712. https://doi.org/10.3390/antibiotics9100712

Silva A, Silva SA, Carpena M, Garcia-Oliveira P, Gullón P, Barroso MF, Prieto MA, Simal-Gandara J. Macroalgae as a Source of Valuable Antimicrobial Compounds: Extraction and Applications. Antibiotics (Basel). 2020;9(10):642. https://doi.org/10.3390/antibiotics9100642

Munir M, Qureshi R, Bibi M, Khan AM. Pharmaceutical aptitude of Cladophora: a comprehensive review. Algal Res. 2019;39:101476. https://doi.org/10.1016/j.algal.2019.101476

Abo-Shady AM, Gheda SF, Ismail GA, Cotas J, Pereira L, Abdel-Karim OH. Antioxidant and Antidiabetic Activity of Algae. Life. 2023;13:460. https://doi.org/10.3390/life13020460

Fabrowska J, Messyasz B, Pankiewicz R, Wilińska P, Łęska B. Seasonal differences in the content of phenols and pigments in thalli of freshwater Cladophora glomerata and its habitat. Water Res. 2018;135:66-74. https://doi.org/10.1016/j.watres.2018.02.020

Schroeder G, Messyasz B, Łęska B. Identification of biologically active compounds and assessment of commercial properties of algal extracts as cosmetic ingredients. In: Chojnacka K, Michalak I, editors. Innovative Bio-Products for Agriculture: Algal Extracts in Products for Humans, Animals and Plants. New York: Nova Science Publisher; 2016.

Michalak I, Chojnacka K, Saeid A. Plant Growth Biostimulants, Dietary Feed Supplements and Cosmetics Formulated with Supercritical CO2 Algal Extracts. Molecules. 2017;22(1):66. https://doi.org/10.3390/molecules22010066

Rico M, González AG, Santana-Casiano M, González-Dávila M, Pérez-Almeida N, de Tangil MS. Production of Primary and Secondary Metabolites Using Algae. In: Tripathi B, Kumar D, editors. Prospects and Challenges in Algal Biotechnology. Singapore: Springer; 2017. p. 311-26. https://doi.org/10.1007/978-981-10-1950-0_12

Nutautaitė M, Vilienė V, Racevičiūtė-Stupelienė A, Bliznikas S, Karosienė J, Koreivienė J. Freshwater Cladophora glomerata Biomass as Promising Protein and Other Essential Nutrients Source for High Quality and More Sustainable Feed Production. Agriculture. 2021;11(7):582. https://doi.org/10.3390/agriculture11070582

Singh M, Gupta N, Gupta P, Doli, Mishra P. Discovery of novel and biologically active compounds from algae. In: Adetunji CO, Oloke JK, Dwivedi N, Beevi S, editors. Next-generation algae Vol 2, Application in Medicine and Pharmaceutical Industry. Scrivener Publishing LLC; 2023. p. 1-40 https://doi.org/10.1002/9781119857860.ch1

Svircev Z, Cetojevic-Simin D, Simeunovic J, Karaman M, Stojanovic D. Antibacterial, antifungal and cytotoxic activity of terrestrial cyanobacterial strains from Serbia. Sci China C Life Sci. 2008;51(10):941-7. https://doi.org/10.1007/s11427-008-0115-8

Babić O, Kovač D, Rašeta M, Šibul F, Svirčev Z, Simeunović J. Evaluation of antioxidant activity and phenolic profile of filamentous terrestrial cyanobacterial strains isolated from forest ecosystem. J Appl Phycol. 2016;8:2333-42. https://doi.org/10.1007/s10811-015-0773-4

Simić S, Kosanić M, Ranković B. Evaluation of In Vitro Antioxidant and Antimicrobial Activities of Green Microalgae Trentepohlia umbrina. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 2012;40:86-91. https://doi.org/10.15835/nbha4027933

Biodiversity of aquatic ecosystems in Serbia, ex situ conservation (BAES ex situ) [Internet]. Kragujevac: Faculty of Science, University of Kragujevac. 2006 - [cited 2024 Jan 17]. Available from: http://baes.pmf.kg.ac.rs

Michalak I, Messyasz B. Concise review of Cladophora spp.: macroalgae of commercial interest. J Appl Phycol. 2021;33:133-66. https://doi.org/10.1007/s10811-020-02211-3

Fabrowska J, Łęska B, Schroeder G. Freshwater Cladophora glomerata as a new potential cosmetic raw material. Chemik. 2015;69(8):491-97.

Messyasz B, Łęska B, Fabrowska J, Pikosz M, Rój E, Cieślak A, Schroeder G. Biomass of freshwater Cladophora as a raw material for agriculture and the cosmetic industry. Open Chem. 2015;13:1108-18. https://doi.org/10.1515/chem-2015-0124

Messyasz B, Michalak I, Leska B, Schroeder G, Górka B, Korzeniowska K, Lipok J, Wieczorek PP, Rój E, Wilk R, Dobrzyńska-Inger A, Górecki H, Chojnacka K. Valuable natural products from marine and freshwater macroalgae obtained from supercritical fluid extracts. J Appl Phycol. 2017;30:591-603. https://doi.org/10.1007/s10811-017-1257-5

Korzeniowska K, Leska B, Wieczorek PP. Isolation and determination of phenolic compounds from freshwater Cladophora glomerata. Algal Res. 2020;48:101912. https://doi.org/10.1016/j.algal.2020.101912

Schagerl M, Kerschbaumer M. Autecology and morphology of selected Vaucheria species (Xanthophyceae). Aquat Ecol. 2009;43:295-03. https://doi.org/10.1007/s10452-007-9163-6

El-Tablawy NH, Mansour HA, Shaaban AEM. Antioxidant activities of some edaphic algae in Egypt. Beni-Suef Univ J Basic Appl Sci. 2020;9:41. https://doi.org/10.1186/s43088-020-00060-0

Iqbal A, Imran M, Badshah SL, Shami A, Ali B, Shah Z, Ayaz M, Alasmari A, Albalawi MA, Al-Doaiss AA, Bajaber MA, Ercisli S. Biochemical profile of Vaucheria karachiensis and evaluation of its nutritional, antioxidant, antimicrobial, and hypoglycemic potentials. Algal Res. 2024;77:103346. https://doi.org/10.1016/j.algal.2023.103346

Meng Y, Yao C, Xue S, Yang H. Application of Fourier transform infrared (FT-IR) spectroscopy in determination of microalgal compositions. Bioresour Technol. 2014;151:347-54. https://doi.org/10.1016/j.biortech.2013.10.064

Lichtenthaler HK. Vegetation stress: an introduction to the stress concept in plants. J Plant Physiol. 1996;148:4-14. https://doi.org/10.1016/S0176-1617(96)80287-2

Wootton-Beard PC, Moran A, Ryan L. Stability of the total antioxidant capacity and total polyphenol content of 23 commercially available vegetable juices before and after in vitro digestion measured by FRAP, DPPH, ABTS and Folin-Ciocalteu methods. Food Res Int. 2011;44(1):217-24. https://doi.org/10.1016/j.foodres.2010.10.033

Takao T, Kitatani F, Watanabe N, Yagi A, Sakata K. A simple screening method for antioxidants and isolation of several antioxidants produced by marine bacteria from fish and shellfish. Bioscience, Biotechnology, and Biochemistry. 1994;58(10):1780-3. https://doi.org/10.1271/bbb.58.1780

Lim TY, Lim YY, Yule CM. Evaluation of antioxidant, antibacterial and antityrosinase activities of four Macaranga species. Food Chem. 2009;114:594-9. https://doi.org/10.1016/j.foodchem.2008.09.093

Clinical and Laboratory Standards Institute (CLSI). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard - Ninth Edition. CLSI document M07-A9, Wayne, Pennsylvania, USA; 2012.

Clinical and Laboratory Standards Institute (CLSI). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeast; Approved Standard-Third Edition. CLSI document M27-A3. Wayne, Pennsylvania, USA; 2008.

Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods. 2000;40:175-9. https://doi.org/10.1016/S0167-7012(00)00122-6

Milutinović M, Stanković M, Cvetković D, Maksimović V, Šmit B, Pavlović R, Marković S. The molecular mechanisms of apoptosis induced by Allium flavum and synergistic effects with new-synthesized Pd(II) complex on colon cancer cells. J Food Biochem. 2015;39(3):238-50. https://doi.org/10.1111/jfbc.12123

Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1-2):55-63. https://doi.org/10.1016/0022-1759(83)90303-4

Nikodijević D, Jovankić J, Cvetković D, Anđelković M, Nikezić A, Milutinović M. L-amino acid oxidase from snake venom: Biotransformation and induction of apoptosis in human colon cancer cells. Eur J Pharmacol. 2021;910(2):174466. https://doi.org/10.1016/j.ejphar.2021.174466

Sukhikh S, Prosekov A, Ivanova S, Maslennikov P, Andreeva A, Budenkova E, Kashirskikh E, Tcibulnikova A, Zemliakova E, Samusev I, Babich O. Identification of Metabolites with Antibacterial Activities by Analyzing the FTIR Spectra of Microalgae. Life. 2022;12(9):1395. https://doi.org/10.3390/life12091395

Grace CEE, Lakshmi PK, Meenakshi S, Vaidyanathan S, Srisudha S, Mary MB. (2020) Biomolecular transitions and lipid accumulation in green microalgae monitored by FTIR and Raman analysis. Spectrochim Acta A Mol Biomol Spectrosc. 2020;224:117382. https://doi.org/10.1016/j.saa.2019.117382

Sarpal A, Teixeira CMLL, Silva PRM, Cunha VS. Biodiesel and Polyunsaturated Fatty Acid (PUFA) Potential of Microalgae Biomass-A Short Review. Res Dev Material Sci. 2019;10(4): RDMS.000744.2019. https://doi.org/10.31031/RDMS.2019.10.000744

Duygu DY, Udoh AU, Ozer TB, Akbulut A, Erkaya IA, Yildiz K, Guler D. Fourier transform infrared (FTIR) spectroscopy for identification of Chlorella vulgaris Beijerinck 1890 and Scenedesmus obliquus (Turpin) Kützing. Afr J Biotechnol. 2012;11(16):3817-24. https://doi.org/10.5897/AJB11.1863

Yarnpakdee S, Benjakul S, Senphan T. Antioxidant activity of the extracts from freshwater macroalgae (Cladophora glomerata) grown in northern Thailand and its preventive effect against lipid oxidation of refrigerated eastern little tuna slice. Turkish J Fish Aquat Sci. 2018;19(3):209-19. https://doi.org/10.4194/1303-2712-v19_3_04

Lawton RJ, de Nys R, Paul NA. Selecting Reliable and Robust Freshwater Macroalgae for Biomass Applications. PLoS One. 2013;8:e64168. https://doi.org/10.1371/journal.pone.0064168

Nutautaitė M, Racevičiūtė-Stupelienė A, Bliznikas S, Jonuškienė I, Karosienė J, Koreivienė J, Vilienė V. Evaluation of Phenolic Compounds and Pigments in Freshwater Cladophora glomerata Biomass from Various Lithuanian Rivers as a Potential Future Raw Material for Biotechnology. Water. 2022;14(7):1138. https://doi.org/10.3390/w14071138

Khuantrairong T, Traichaiyaporn S. The nutritional value of edible freshwater alga Cladophora sp. (Chlorophyta) grown under different phosphorus concentrations. Int J Agric Biol. 2011;13:297-300.

Shah Z, Badshah SL, Iqbal A, Shah Z, Emwas AH, Jaremko M. Investigation of important biochemical compounds from selected freshwater macroalgae and their role in agriculture. Chem Biol Technol Agric. 2022;9:9. https://doi.org/10.1186/s40538-021-00273-0

Goud JP, Charya S. Antibacterial activity and biomolecular composition of certain freshwater microalgae from river Godavari (India). Int J Algae. 2007;9:350-58. https://doi.org/10.1615/InterJAlgae.v9.i4.40

Forman HJ, Zhang H. Targeting oxidative stress in disease: Promise and limitations of antioxidant therapy. Nat Rev Drug Discov. 2021;20:689-709. https://doi.org/10.1038/s41573-021-00233-1

Lourenço SC, Moldão-Martins M, Alves VD. Antioxidants of Natural Plant Origins: From Sources to Food Industry Applications. Molecules. 2019;24:4132. https://doi.org/10.3390/molecules24224132

Rahaman MM, Hossain R, Herrera-Bravo J, Islam MT, Atolani O, Adeyemi OS, Owolodun OA, Kambizi L, Daştan SD, Calina D, Sharifi-Rad J. Natural antioxidants from some fruits, seeds, foods, natural products, and associated health benefits: An update. Food Sci Nutr. 2023;13;11(4):1657-70. https://doi.org/10.1002/fsn3.3217

Laungsuwon R, Chulalaksananukul W. Antioxidant and anticancer activities of freshwater green algae, Cladophora glomerata and Microspora floccosa, from Nan River in northern Thailand. Maejo Int J Sci TechnoL. 2013;7(2):181-8.

Amornlerdpison D, Mengumphan K, Thumvijit S, Peerapornpisal Y. Antioxidant and anti-inflammatory activities of freshwater macroalga, Cladophora glomerata Kützing. Thai J Agric ScI. 2011;44(5):283-91.

Bourebaba L, Michalak I, Röcken M, Marycz K. Cladophora glomerata methanolic extract decreases oxidative stress and improves viability and mitochondrial potential in equine adipose derived mesenchymal stem cells (ASCs). Biomed Pharmacother. 2019;111:6-18. https://doi.org/10.1016/j.biopha.2018.12.020

Ali RAAR, Dwaish AS. Antibacterial Activity and Qualitative Phytochemical Analysis of Cladophora glomerate. Int J Pharm Qual Assur. 2018;9(2):120-3. https://doi.org/10.25258/ijpqa.v9i2.13633

Yuvaraj N, Kanmani P, Satishkumar R, Paari KA, Pattukumar V, Arul V. Extraction, purification and partial characterization of Cladophora glomerata against multidrug resistant human pathogen Acinetobacter baumannii and fish pathogens. World J Fish Mar Sci. 2011;3:51-7.

El-Adl MF, Deyab MA, El-Shanawany RS, Abu Ahmed SE. Fatty acids of Cladophora glomerata and Chaetomorpha vieillardii (Cladophoraceae) of different niches inhibit the pathogenic microbial growth. Aquat Bot. 2022;176:103461. https://doi.org/10.1016/j.aquabot.2021.103461

Laungsuwon R, Chulalaksananukul W. Chemical composition and antibacterial activity of extracts of freshwater green algae, Cladophora glomerata Kützing and Microspora floccosa (Vaucher) Thuret. J Biosci Biotechnol. 2014;3(3):211-8.

Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 2016;14(9):563-75. https://doi.org/10.1038/nrmicro.2016.94

Fayyad RJ, Mohammed Ali AN, Saeed AHA, Hamzah IH, Dwaish AS. Phycosynthesis of Silver Nanoparticles Using Cladophora Glomerata and Evaluation of Their Ability to Inhibit the Proliferation of MCF-7 and L20B Cell Lines. Asian Pac J Cancer Prev. 2022;23(10):3563-9. https://doi.org/10.31557/APJCP.2022.23.10.3563

Sundaramoorthy S, Dakshinamoorthi A, Chithra K. Evaluation of antioxidant and anticancer effect of marine algae Cladophora glomerata in HT29 colon cancer cell lines- an in-vitro study. Int J Physiol Pathophysiol Pharmacol. 2022;14(6):332-9.

Bézivin C, Tomasi S, Lohézic-Le Dévéhat F, Boustie, J. Cytotoxic activity of some lichen extracts on murine and human cancer cell lines. Phytomedicine. 2003;10(6-7):499-503. https://doi.org/10.1078/094471103322331458

Downloads

Published

2024-07-10

How to Cite

1.
Stefanović OD, Rakonjac AB, Nikodijević DD, Milojević SD, Dinić A, Simić SB. Freshwater algae Cladophora glomerata and Vaucheria sp. from Serbia as sources of bioactive compounds: chemical analysis and biological activities. Arch Biol Sci [Internet]. 2024Jul.10 [cited 2024Dec.22];76(2):175-89. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/9549

Issue

Section

Articles