Generic placeholder image

Current Pharmaceutical Biotechnology

Author(s): Doaa Abdullah Hammadi Al-Ogaidi, Sevinç Karaçam, Rafig Gurbanov and Nurcan Vardar-Yel*

DOI: 10.2174/0113892010291960240223054911

DownloadDownload PDF Flyer Cite As
Marine Microalgae Schizochytrium sp. S31: Potential Source for New Antimicrobial and Antibiofilm Agent

Page: [1478 - 1488] Pages: 11

  • * (Excluding Mailing and Handling)

Abstract

Background: The rise of antibiotic-resistant bacteria necessitates the discovery of new, safe, and bioactive antimicrobial compounds. The antibacterial and antibiofilm activity of microalgae makes them a potential candidate for developing natural antibiotics to limit microbial infection in various fields.

Objective: This study aimed to analyze the antibacterial effect of the methanolic extract of Schizochytrium sp. S31 microalgae by broth microdilution and spot plate assays.

Methods: The antibacterial effects of Schizochytrium sp. S31 extract was studied on gramnegative pathogens, Pseudomonas aeruginosa, Escherichia coli 35218, Klebsiella pneumonia, which cause many different human infections, and the gram-positive pathogen Streptococcus mutans. At the same time, the antibiofilm activity of the Schizochytrium sp. S31 extract on Pseudomonas aeruginosa and Escherichia coli 35218 bacteria were investigated by crystal violet staining method.

Results: Schizochytrium sp. S31 extract at a 60% concentration for 8 hours displayed the highest antibacterial activity against P. aeruginosa, E. coli 35218, and K. pneumonia, with a decrease of 87%, 92%, and 98% in cell viability, respectively. The experiment with Streptococcus mutans revealed a remarkable antibacterial effect at a 60% extract concentration for 24 hours, leading to a notable 93% reduction in cell viability. Furthermore, the extract exhibited a dose-dependent inhibition of biofilm formation in P. aeruginosa and E. coli 35218. The concentration of 60% extract was identified as the most effective dosage in terms of inhibition.

Conclusion: This research emphasizes the potential of Schizochytrium sp. S31 as a natural antibacterial and antibiofilm agent with promising applications in the pharmaceutical sectors. This is the first study to examine the antibacterial activity of Schizochytrium sp. S31 microalgae using broth microdilution, spot plate assays, and the antibiofilm activity by a crystal staining method. The findings of this study show that Schizochytrium sp. S31 has antibacterial and antibiofilm activities against critical bacterial pathogens.

Graphical Abstract

[1]
Khavari, F.; Saidijam, M.; Taheri, M.; Nouri, F. Microalgae: Therapeutic potentials and applications. Mol. Biol. Rep., 2021, 48(5), 4757-4765.
[http://dx.doi.org/10.1007/s11033-021-06422-w] [PMID: 34028654]
[2]
Sigamani, S.; Ramamurthy, D.; Natarajan, H. A review on potential biotechnological applications of microalgae. J. Appl. Pharm. Sci., 2016, 6(8), 179-184.
[http://dx.doi.org/10.7324/JAPS.2016.60829]
[3]
Chu, W.L.; Phang, S.M. Bioactive compounds from microalgae and their potential applications as pharmaceuticals and nutraceuticals. In: Grand Challenges in Algae Biotechnology; Hallmann, A.; Rampelotto, P., Eds.; Springer: Cham, 2019; pp. 429-469.
[http://dx.doi.org/10.1007/978-3-030-25233-5_12]
[4]
Dhandayuthapani, K.; Malathy, S.; Mulla, S.I.; Gupta, S.K. An insight into the potential application of microalgae in pharmaceutical and nutraceutical production. In: Algae Multifarious Applications for a Sustainable World; Mandotra, S.K.; Upadhyay, A.K.; Ahluwalia, A.S., Eds.; Springer: Singapore, 2021; pp. 135-179.
[http://dx.doi.org/10.1007/978-981-15-7518-1_7]
[5]
Olasehinde, T.; Olaniran, A.; Okoh, A. Therapeutic potentials of microalgae in the treatment of Alzheimer’s disease. Molecules, 2017, 22(3), 480.
[http://dx.doi.org/10.3390/molecules22030480] [PMID: 28335462]
[6]
Jubair, N.; Rajagopal, M.; Chinnappan, S.; Abdullah, N.B.; Fatima, A. Review on the antibacterial mechanism of plant-derived compounds against multidrug-resistant bacteria (MDR). Evid. Based Complement. Alternat. Med., 2021, 2021, 3663315.
[http://dx.doi.org/10.1155/2021/3663315]
[7]
Prestinaci, F.; Pezzotti, P.; Pantosti, A. Antimicrobial resistance: A global multifaceted phenomenon. Pathog. Glob. Health, 2015, 109(7), 309-318.
[http://dx.doi.org/10.1179/2047773215Y.0000000030] [PMID: 26343252]
[8]
Kon, K.; Rai, M. Antibiotic Resistance: Mechanisms and New Antimicrobial Approaches; Academic press: London, 2016.
[9]
Marrez, D.A.; Naguib, M.M.; Sultan, Y.Y.; Higazy, A.M. Antimicrobial and anticancer activities of Scenedesmus obliquus metabolites. Heliyon, 2019, 5(3), e01404.
[http://dx.doi.org/10.1016/j.heliyon.2019.e01404] [PMID: 30976685]
[10]
Shannon, E.; Abu-Ghannam, N. Antibacterial derivatives of marine algae: An overview of pharmacological mechanisms and applications. Mar. Drugs, 2016, 14(4), 81.
[http://dx.doi.org/10.3390/md14040081] [PMID: 27110798]
[11]
Vikneshan, M.; Saravanakumar, R.; Mangaiyarkarasi, R.; Rajeshkumar, S.; Samuel, S.R.; Suganya, M.; Baskar, G. Algal biomass as a source for novel oral nano-antimicrobial agent. Saudi J. Biol. Sci., 2020, 27(12), 3753-3758.
[http://dx.doi.org/10.1016/j.sjbs.2020.08.022] [PMID: 33304187]
[12]
Stirk, W.A.; van Staden, J. Bioprospecting for bioactive compounds in microalgae: Antimicrobial compounds. Biotechnol. Adv., 2022, 59, 107977.
[http://dx.doi.org/10.1016/j.biotechadv.2022.107977] [PMID: 35580750]
[13]
Ruiz, M.M.; González, M.C.A.; Kim, D.H.; Romero, S.B.; Pardo, R.H.; Zepeda, V.K.R.; Sánchez, M.E.R.; Gamboa, R.D.; Zamorano, D.A.L.; Hernández, S.J.E.; Apodaca, C.K.G.; Méndez, G.A.M.; Iqbal, H.M.N.; Saldivar, P.R. Microalgae bioactive compounds to topical applications products—a review. Molecules, 2022, 27(11), 3512.
[http://dx.doi.org/10.3390/molecules27113512] [PMID: 35684447]
[14]
de Morais, M.G.; Vaz, B.S.; de Morais, E.G.; Costa, J.A.V. Biologically active metabolites synthesized by microalgae. BioMed Res. Int., 2015, 2015, 1-15.
[http://dx.doi.org/10.1155/2015/835761] [PMID: 26339647]
[15]
Das, B.K.; Pradhan, J. Antibacterial properties of selected freshwater microalgae against pathogenic bacteria. Indian J. Fish., 2010, 57(2), 61-66.
[16]
Jyotirmayee, P.; Sachidananda, D.; Basanta, K.D. Antibacterial activity of freshwater microalgae: A review. Afr. J. Pharm. Pharmacol., 2014, 8(32), 809-818.
[http://dx.doi.org/10.5897/AJPP2013.0002]
[17]
Jena, J.; Subudhi, E. Microalgae: An untapped resource for natural antimicrobials. In: The Role of Microalgae in Wastewater Treatment; Sukla, L.; Subudhi, E.; Pradhan, D., Eds.; Springer Singapore, 2019; pp. 99-114.
[http://dx.doi.org/10.1007/978-981-13-1586-2_8]
[18]
Mayer, A.M.S.; Hamann, M.T. Marine pharmacology in 2001–2002: Marine compounds with anthelmintic, antibacterial, anticoagulant, antidiabetic, antifungal, anti-inflammatory, antimalarial, antiplatelet, antiprotozoal, antituberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems and other miscellaneous mechanisms of action. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2005, 140(3-4), 265-286.
[http://dx.doi.org/10.1016/j.cca.2005.04.004] [PMID: 15919242]
[19]
Surendhiran, D.; Vijay, M.; Sirajunnisa, A.R.; Subramaniyan, T.; Subramaniyan, A.S.; Tamilselvam, K. A green synthesis of antimicrobial compounds from marine microalgae Nannochloropsis oculata. J. Coast. Life Med., 2014, 2(11), 862-869.
[20]
Bhateja, P.; Mathur, T.; Pandya, M.; Fatma, T.; Rattan, A. Activity of blue green microalgae extracts against in vitro generated Staphylococcus aureus with reduced susceptibility to vancomycin. Fitoterapia, 2006, 77(3), 233-235.
[http://dx.doi.org/10.1016/j.fitote.2006.01.009] [PMID: 16556488]
[21]
Amaro, H.M.; Guedes, A.C.; Malcata, F.; Guedes, A.C.; Malcata, F.X. Antimicrobial activities of microalgae: An invited review. In: Science against microbial pathogens: communicating current research and technological advances; Méndez-Vilas, A., Ed.; Formatex: Spain, 2011; pp. 1272-1284.
[22]
Cepas, V.; López, Y.; Gabasa, Y.; Martins, C.B.; Ferreira, J.D.; Correia, M.J.; Santos, L.M.A.; Oliveira, F.; Ramos, V.; Reis, M.; Branco, C.R.; Morais, J.; Vasconcelos, V.; Probert, I.; Guilloud, E.; Mehiri, M.; Soto, S.M. Inhibition of bacterial and fungal biofilm formation by 675 extracts from microalgae and cyanobacteria. Antibiotics, 2019, 8(2), 77.
[http://dx.doi.org/10.3390/antibiotics8020077] [PMID: 31212792]
[23]
Kanimozhi, R.; Prasath, D.A.; Dhandapani, R.; Sigamani, S. In vitro antioxidant and antibiofilm activities of microcystis sp. against multidrug-resistant human pathogens. Ann. Rom. Soc. Cell Biol., 2021, 25(6), 4419-4430.
[24]
Mishra, A.K.R.; Muthukaliannan, K.G. Role of microalgal metabolites in controlling quorum-sensing-regulated biofilm. Arch. Microbiol., 2022, 204(3), 163.
[http://dx.doi.org/10.1007/s00203-022-02776-2] [PMID: 35119531]
[25]
Sampathkumar, S.J.; Srivastava, P.; Ramachandran, S.; Sivashanmugam, K.; Gothandam, K.M. Lutein: A potential antibiofilm and antiquorum sensing molecule from green microalga Chlorella pyrenoidosa. Microb. Pathog., 2019, 135, 103658.
[http://dx.doi.org/10.1016/j.micpath.2019.103658] [PMID: 31398531]
[26]
Iglesias, M.J.; Soengas, R.; Probert, I.; Guilloud, E.; Gourvil, P.; Mehiri, M.; López, Y.; Cepas, V.; del-Río, G.I.; Blanco, R.S.; Villar, C.J.; Lombó, F.; Soto, S.; Ortiz, F.L. NMR characterization and evaluation of antibacterial and antiobiofilm activity of organic extracts from stationary phase batch cultures of five marine microalgae (Dunaliella sp., D. salina, Chaetoceros calcitrans, C. gracilis and Tisochrysis lutea). Phytochemistry, 2019, 164, 192-205.
[http://dx.doi.org/10.1016/j.phytochem.2019.05.001] [PMID: 31174083]
[27]
Cosio, C.P.; Escalante, M.E.; Geraldo, R.R.; Angulo, C. Natural and recombinant bioactive compounds from Schizochytrium sp.: Recent advances and future prospects. Algal Res., 2023, 75, 103273.
[http://dx.doi.org/10.1016/j.algal.2023.103273]
[28]
Nag, M.; Lahiri, D.; Dey, A.; Sarkar, T.; Joshi, S.; Ray, R.R. Evaluation of algal active compounds as potent antibiofilm agent. J. Basic Microbiol., 2022, 62(9), 1098-1109.
[http://dx.doi.org/10.1002/jobm.202100470] [PMID: 34939676]
[29]
Puri, M.; Gupta, A.; Sahni, S. Schizochytrium sp. In: Trends in Microbiology; Iyer, S., Ed.; Elsevier, 2023; pp. 872-873.
[30]
Wang, Q.; Han, W.; Jin, W.; Gao, S.; Zhou, X. Docosahexaenoic acid production by Schizochytrium sp.: review and prospect. Food Biotechnol., 2021, 35(2), 111-135.
[http://dx.doi.org/10.1080/08905436.2021.1908900]
[31]
Półbrat, T.; Konkol, D.; Korczyński, M. Optimization of docosahexaenoic acid production by Schizochytrium SP. – A review. Biocatal. Agric. Biotechnol., 2021, 35, 102076.
[http://dx.doi.org/10.1016/j.bcab.2021.102076]
[32]
FDA. Substances affirmed as generally recognized as safe: Algal Oil (Schizochytrium sp.). GRN no. 137. 2004. Available from: https://www.fda.gov/food/generally-recognized-safe-gras/gras-notice-inventory
[33]
Lewis, K.D.; Huang, W.; Zheng, X.; Jiang, Y.; Feldman, R.S.; Falk, M.C. Toxicological evaluation of arachidonic acid (ARA)-rich oil and docosahexaenoic acid (DHA)-rich oil. Food Chem. Toxicol., 2016, 96, 133-144.
[http://dx.doi.org/10.1016/j.fct.2016.07.026] [PMID: 27470615]
[34]
Hammond, B.G.; Mayhew, D.A.; Robinson, K.; Mast, R.W.; Sander, W.J. Safety assessment of DHA-rich microalgae from Schizochytrium sp. Part III. Single generation rat reproduction study. Regul. Toxicol. Pharmacol., 2001, 33(3), 356-362.
[http://dx.doi.org/10.1006/rtph.2001.1477] [PMID: 11407938]
[35]
Hammond, B.G.; Mayhew, D.A.; Naylor, M.W.; Ruecker, F.A.; Mast, R.W.; Sander, W.J. Safety assessment of DHA-rich microalgae from Schizochytrium Sp.: I. Subchronic rat feeding study. Regul. Toxicol. Pharmacol., 2001, 33(2), 192-204.
[http://dx.doi.org/10.1006/rtph.2001.1458] [PMID: 11350202]
[36]
Hammond, B.G.; Mayhew, D.A.; Holson, J.F.; Nemec, M.D.; Mast, R.W.; Sander, W.J. Safety assessment of DHA-rich microalgae from Schizochytrium sp.: II. Developmental toxicity evaluation in rats and rabbits. Regul. Toxicol. Pharmacol., 2001, 33(2), 205-217.
[http://dx.doi.org/10.1006/rtph.2001.1459] [PMID: 11350203]
[37]
Abril, R.; Garrett, J.; Zeller, S.G.; Sander, W.J.; Mast, R.W. Safety assessment of DHA-rich microalgae from Schizochytrium sp. Part V: target animal safety/toxicity study in growing swine. Regul. Toxicol. Pharmacol., 2003, 37(1), 73-82.
[http://dx.doi.org/10.1016/S0273-2300(02)00030-2] [PMID: 12662911]
[38]
Dahms, F.I.; Marone, P.A.; Hall, B.E.; Ryan, A.S. Safety evaluation of algal oil from Schizochytrium sp. Food Chem. Toxicol., 2011, 49(1), 70-77.
[http://dx.doi.org/10.1016/j.fct.2010.09.033] [PMID: 20933569]
[39]
Arterburn, L.M.; Boswell, K.D.; Lawlor, T.; Cifone, M.A.; Murli, H.; Kyle, D.J. In vitro genotoxicity testing of ARASCO® and DHASCO® oils. Food Chem. Toxicol., 2000, 38(11), 971-976.
[http://dx.doi.org/10.1016/S0278-6915(00)00085-5] [PMID: 11038233]
[40]
Schmitt, D.; Tran, N.; Peach, J.; Bauter, M.; Marone, P. Toxicologic evaluation of DHA-rich algal oil: Genotoxicity, acute and subchronic toxicity in rats. Food Chem. Toxicol., 2012, 50(10), 3567-3576.
[http://dx.doi.org/10.1016/j.fct.2012.07.054] [PMID: 22898615]
[41]
Kroes, R.; Schaefer, E.J.; Squire, R.A.; Williams, G.M. A review of the safety of DHA45-oil. Food Chem. Toxicol., 2003, 41(11), 1433-1446.
[http://dx.doi.org/10.1016/S0278-6915(03)00163-7] [PMID: 12962995]
[42]
Blum, R.; Kiy, T.; Tanaka, S.; Wong, A.W.; Roberts, A. Genotoxicity and subchronic toxicity studies of DHA-rich oil in rats. Regul. Toxicol. Pharmacol., 2007, 49(3), 271-284.
[http://dx.doi.org/10.1016/j.yrtph.2007.08.005] [PMID: 17933446]
[43]
Sahin, D.; Tas, E.; Altindag, U.H. Enhancement of docosahexaenoic acid (DHA) production from Schizochytrium sp. S31 using different growth medium conditions. AMB Express, 2018, 8(1), 7.
[http://dx.doi.org/10.1186/s13568-018-0540-4] [PMID: 29368055]
[44]
Karadağ H.; Tunçer, S.; Karaçam, S.; Gurbanov, R. Tapioca starch and skim milk support probiotic efficacy of Lactiplantibacillus plantarum post-fermentation medium against pathogens and cancer cells. Arch. Microbiol., 2022, 204(6), 331.
[http://dx.doi.org/10.1007/s00203-022-02943-5] [PMID: 35579801]
[45]
Merritt, J.H.; Kadouri, D.E.; O’Toole, G.A. Growing and analyzing static biofilms. Curr. Protoc. Microbiol., 2011, 22(1), 1B-1.
[http://dx.doi.org/10.1002/9780471729259.mc01b01s22] [PMID: 18770545]
[46]
Tunçer, S.; Karaçam, S. Cell-free supernatant of Streptococcus salivarius M18 impairs the pathogenic properties of Pseudomonas aeruginosa and Klebsiella pneumonia. Arch. Microbiol., 2020, 202(10), 2825-2840.
[http://dx.doi.org/10.1007/s00203-020-02005-8] [PMID: 32747998]
[47]
Cepas, V.; Río, G.D.I.; López, Y.; Blanco, R.S.; Gabasa, Y.; Iglesias, M.J.; Soengas, R.; Lorenzo, F.A.; Ibáñez, L.S.; Villar, C.J.; Martins, C.B.; Ferreira, J.D.; Assunção, M.F.G.; Santos, L.M.A.; Morais, J.; Branco, C.R.; Reis, M.A.; Vasconcelos, V.; Ortiz, L.F.; Lombó, F.; Soto, S.M. Microalgae and cyanobacteria strains as producers of lipids with antibacterial and antibiofilm activity. Mar. Drugs, 2021, 19(12), 675.
[http://dx.doi.org/10.3390/md19120675] [PMID: 34940674]
[48]
Blackledge, M.S.; Worthington, R.J.; Melander, C. Biologically inspired strategies for combating bacterial biofilms. Curr. Opin. Pharmacol., 2013, 13(5), 699-706.
[http://dx.doi.org/10.1016/j.coph.2013.07.004] [PMID: 23871261]
[49]
Flemming, H.C.; Wuertz, S. Bacteria and archaea on earth and their abundance in biofilms. Nat. Rev. Microbiol., 2019, 17(4), 247-260.
[http://dx.doi.org/10.1038/s41579-019-0158-9] [PMID: 30760902]
[50]
Khatoon, Z.; McTiernan, C.D.; Suuronen, E.J.; Mah, T.F.; Alarcon, E.I.; Bacterial, A.E.I. Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon, 2018, 4(12), e01067.
[http://dx.doi.org/10.1016/j.heliyon.2018.e01067] [PMID: 30619958]
[51]
Sauer, K.; Stoodley, P.; Goeres, D.M.; Stoodley, H.L.; Burmølle, M.; Stewart, P.S.; Bjarnsholt, T. The biofilm life cycle: Expanding the conceptual model of biofilm formation. Nat. Rev. Microbiol., 2022, 20(10), 608-620.
[http://dx.doi.org/10.1038/s41579-022-00767-0] [PMID: 35922483]
[52]
Muhammad, M.H.; Idris, A.L.; Fan, X.; Guo, Y.; Yu, Y.; Jin, X.; Qiu, J.; Guan, X.; Huang, T. Beyond risk: Bacterial biofilms and their regulating approaches. Front. Microbiol., 2020, 11, 928.
[http://dx.doi.org/10.3389/fmicb.2020.00928] [PMID: 32508772]
[53]
Aslam, B.; Wang, W.; Arshad, M.I.; Khurshid, M.; Muzammil, S.; Rasool, M.H.; Nisar, M.A.; Alvi, R.F.; Aslam, M.A.; Qamar, M.U.; Salamat, M.K.F.; Baloch, Z. Antibiotic resistance: A rundown of a global crisis. Infect. Drug Resist., 2018, 11, 1645-1658.
[http://dx.doi.org/10.2147/IDR.S173867] [PMID: 30349322]
[54]
Rojas, V.; Rivas, L.; Cárdenas, C.; Guzmán, F. Cyanobacteria and eukaryotic microalgae as emerging sources of antibacterial peptides. Molecules, 2020, 25(24), 5804.
[http://dx.doi.org/10.3390/molecules25245804] [PMID: 33316949]
[55]
López, Y.; Soto, S.M. The preventing usefulness biofilm microalgae infections compounds for preventing biofilm infections. Antibiotics, 2020, 9, 9.
[http://dx.doi.org/10.3390/antibiotics9010009] [PMID: 31878164]
[56]
Dolganyuk, V.; Belova, D.; Babich, O.; Prosekov, A.; Ivanova, S.; Katserov, D.; Patyukov, N.; Sukhikh, S. Microalgae: A promising source of valuable bioproducts. Biomolecules, 2020, 10(8), 1153.
[http://dx.doi.org/10.3390/biom10081153] [PMID: 32781745]
[57]
Falaise, C.; François, C.; Travers, M.A.; Morga, B.; Haure, J.; Tremblay, R.; Turcotte, F.; Pasetto, P.; Gastineau, R.; Hardivillier, Y.; Leignel, V.; Mouget, J.L. Antimicrobial compounds from eukaryotic microalgae against human pathogens and diseases in aquaculture. Mar. Drugs, 2016, 14(9), 159.
[http://dx.doi.org/10.3390/md14090159] [PMID: 27598176]
[58]
Lyczak, J.B.; Cannon, C.L.; Pier, G.B. Establishment of Pseudomonas aeruginosa infection: Lessons from a versatile opportunist. Microbes Infect., 2000, 2(9), 1051-1060.
[http://dx.doi.org/10.1016/S1286-4579(00)01259-4] [PMID: 10967285]
[59]
Gellatly, S.L.; Hancock, R.E.W. Pseudomonas aeruginosa: New insights into pathogenesis and host defenses. Pathog. Dis., 2013, 67(3), 159-173.
[http://dx.doi.org/10.1111/2049-632X.12033] [PMID: 23620179]
[60]
Caneiras, C.; Lito, L.; Cristino, M.J.; Duarte, A. Community-and hospital-acquired Klebsiella pneumoniae urinary tract infections in Portugal: Virulence and antibiotic resistance. Microorganisms, 2019, 7(5), 138.
[http://dx.doi.org/10.3390/microorganisms7050138] [PMID: 31100810]
[61]
Azimi, L.; Alaghehbandan, R.; Asadian, M.; Alinejad, F.; Lari, A.R. Multi-drug resistant Pseudomonas aeruginosa and Klebsiella pneumoniae circulation in a burn hospital, Tehran, Iran. GMS Hyg. Infect. Control, 2019, 14, Doc01.
[http://dx.doi.org/10.3205/dgkh000317]
[62]
Zhang, S.; Yang, G.; Ye, Q.; Wu, Q.; Zhang, J.; Huang, Y. Phenotypic and genotypic characterization of Klebsiella pneumoniae isolated from retail foods in China. Front. Microbiol., 2018, 9, 289.
[http://dx.doi.org/10.3389/fmicb.2018.00289] [PMID: 29545778]
[63]
Zhou, F.; Wang, D.; Hu, J.; Zhang, Y.; Tan, B.K.; Lin, S. Control measurements of Escherichia coli biofilm: A review. Foods, 2022, 11(16), 2469.
[http://dx.doi.org/10.3390/foods11162469] [PMID: 36010469]
[64]
Metwalli, K.H.; Khan, S.A.; Krom, B.P.; Rizk, J.M.A. Streptococcus mutans, Candida albicans, and the human mouth: A sticky situation. PLoS Pathog., 2013, 9(10), e1003616.
[http://dx.doi.org/10.1371/journal.ppat.1003616] [PMID: 24146611]
[65]
Chanda, W.; Joseph, T.P.; Guo, X.; Wang, W.; Liu, M.; Vuai, M.S.; Padhiar, A.A.; Zhong, M. Effectiveness of omega-3 polyunsaturated fatty acids against microbial pathogens. J. Zhejiang Univ. Sci. B, 2018, 19(4), 253-262.
[http://dx.doi.org/10.1631/jzus.B1700063] [PMID: 29616501]
[66]
Kalidasan, K.; Sunil, K.; Kayalvizhi, K.; Kathiresan, K. Polyunsaturated fatty acid-producing marine thraustochytrids: A potential source for antimicrobials. J. Coast. Life Med., 2015, 3(11), 848-851.
[http://dx.doi.org/10.12980/jclm.3.2015j5-75]
[67]
Huber, C.D.C.; Steixner, S.; Wurm, A.; Nogler, M. Antibacterial and anti-biofilm activity of omega-3 polyunsaturated fatty acids against periprosthetic joint infections-isolated multi-drug resistant strains. Biomedicines, 2021, 9(4), 334.
[http://dx.doi.org/10.3390/biomedicines9040334] [PMID: 33810261]
[68]
Desbois, A.; Lawlor, K. Antibacterial activity of long-chain polyunsaturated fatty acids against Propionibacterium acnes and Staphylococcus aureus. Mar. Drugs, 2013, 11(11), 4544-4557.
[http://dx.doi.org/10.3390/md11114544] [PMID: 24232668]
[69]
Som, C.R.S.; Radhakrishnan, C.K. Antibacterial activities of polyunsaturated fatty acid extracts from Sardinella longiceps and Sardinella fimbriata. IJMS, 2011, 40(5), 710-716.
[70]
Knapp, H.R.; Melly, M.A. Bactericidal effects of polyunsaturated fatty acids. J. Infect. Dis., 1986, 154(1), 84-94.
[http://dx.doi.org/10.1093/infdis/154.1.84] [PMID: 3086465]
[71]
Zheng, C.J.; Yoo, J.S.; Lee, T.G.; Cho, H.Y.; Kim, Y.H.; Kim, W.G. Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Lett., 2005, 579(23), 5157-5162.
[http://dx.doi.org/10.1016/j.febslet.2005.08.028] [PMID: 16146629]
[72]
Alsenani, F.; Tupally, K.R.; Chua, E.T.; Eltanahy, E.; Alsufyani, H.; Parekh, H.S.; Schenk, P.M. Evaluation of microalgae and cyanobacteria as potential sources of antimicrobial compounds. Saudi Pharm. J., 2020, 28(12), 1834-1841.
[http://dx.doi.org/10.1016/j.jsps.2020.11.010] [PMID: 33424272]
[73]
Smith, V.J.; Desbois, A.P.; Dyrynda, E.A. Conventional and unconventional antimicrobials from fish, marine invertebrates and micro-algae. Mar. Drugs, 2010, 8(4), 1213-1262.
[http://dx.doi.org/10.3390/md8041213] [PMID: 20479976]
[74]
Desbois, A.P.; Lebl, T.; Yan, L.; Smith, V.J. Isolation and structural characterisation of two antibacterial free fatty acids from the marine diatom, Phaeodactylum tricornutum. Appl. Microbiol. Biotechnol., 2008, 81(4), 755-764.
[http://dx.doi.org/10.1007/s00253-008-1714-9] [PMID: 18813920]
[75]
Plaza, M.; Santoyo, S.; Jaime, L.; Reina, G.B.G.; Herrero, M.; Señoráns, F.J.; Ibáñez, E. Screening for bioactive compounds from algae. J. Pharm. Biomed. Anal., 2010, 51(2), 450-455.
[http://dx.doi.org/10.1016/j.jpba.2009.03.016] [PMID: 19375880]