Awards Nomination 20+ Million Readerbase
Indexed In
  • Online Access to Research in the Environment (OARE)
  • Open J Gate
  • Genamics JournalSeek
  • JournalTOCs
  • Scimago
  • Ulrich's Periodicals Directory
  • Access to Global Online Research in Agriculture (AGORA)
  • Electronic Journals Library
  • Centre for Agriculture and Biosciences International (CABI)
  • RefSeek
  • Directory of Research Journal Indexing (DRJI)
  • Hamdard University
  • EBSCO A-Z
  • OCLC- WorldCat
  • Scholarsteer
  • SWB online catalog
  • Virtual Library of Biology (vifabio)
  • Publons
  • MIAR
  • University Grants Commission
  • Euro Pub
  • Google Scholar
Share This Page
Journal Flyer
Flyer image

Short Communication - (2014) Volume 5, Issue 3

Bioactive Compounds Derived from Microalgae Showing Antimicrobial Activities

Swapnil Sanmukh1, Benedict Bruno1, Udhaya Ramakrishnan1, Krishna Khairnar2*, Sandhya Swaminathan1 and Waman Paunikar2
1NEERI Zonal Laboratory, CSIR Complex, Taramani., Chennai 600113, Tamil Nadu, India, E-mail: swamukh1985in@rediffmail.com
2Environmental Virology Cell, National Environmental Engineering Research Institute (NEERI), Nehru Marg, Nagpur-440020, Maharashtra, India, E-mail: swamukh1985in@rediffmail.com
*Corresponding Author: Krishna Khairnar, NEERI Zonal Laboratory, CSIR Complex, Taramani., Chennai 600113, Tamil Nadu, India, Tel: 09890682388 Email:

Abstract

Microalgae have been explored for their bioactive compounds with promising applications encompassing
antibacterial, antiviral, antifungal and antialgal activities. Considering the present status of widely used treatment therapies and their limitations to tackle their adverse effects, the application of bioactive compounds derived from algae will prove beneficial and much more effective as compared with traditional treatment methods. Due to the emerging infectious diseases, viral infections (epidemic and pandemic) and raise in antibiotic resistant bacteria, there is an urgent need for development of alternative treatment therapies against infectious diseases. Present work provides a brief introduction about the algal bioactive compounds and their activities against various pathogens.

Keywords: Microalgae; Antibacterial; Antifungal; Antiviral

Introduction

Algae has wide span of ecosystems contributes to the innumerable antimicrobial compounds have been identified in miceoalgae as well as macroalgae [1]. More than 18,000 new compounds have been isolated from marine sources, yet majority of them have not yet been obtained nor characterized [2]. Therefore, microalgae represent a unique opportunity to discover novel metabolites. The rate of finding metabolites already obtained from other biological sources is less in microalgae as compared with other microorganisms [3]. Due to their metabolic plasticity under stressed vs. nonstressed conditions microalgae possess the extra advantage of triggering secondary metabolism [4]. As microalgae where potentially explored only after 1950s, they were not considered previously for therapeutic purposes. Extensive search is presently undergoing to find novel therapeutically useful agents [5-7]. Microalgae have meanwhile been found to produce antibiotics. A large number of microalgal extracts and/or extracellular products have proven antibacterial, antifungal, antiprotozoal and antiplasmodial [6-13]. Efforts to identify the compounds directly responsible for those antimicrobial features have been made, but are still embryonic.

We have been working with algae like Chlorella and Chlamydomonas (Figure 1) isolated, maintained and extracted as described by Salem et al. [14]. These extracts were later used for antibacterial assay and determination of minimum inhibition concentration (MIC). Antibacterial activity of algal extracts determines the MIC of algae used in this study in vitro [14].

aquaculture-research-development-microscopic-images

Figure 1: The microscopic images of chlorella sp. (1) and Chlamydomonas sp. (2).

Algal cell-free extracts are already being tested [15-17]. Our aim is to provide information about the recent trends in the discovery of bioactive compounds derived from algae which have shown their potential as antimicrobial agents. We have briefly summarized the recent works carried out by the researchers globally in the field of algal antimicrobial activities.

Antimicrobial activities of algal extracts

Antibacterial activity of algae: The needs for development of alternative antibiotic agent were investigated since the emergence of antibiotic resistant microbes. Due to the emergence of drugresistant pathogens they endanger people in affluent, industrial societies like the United States, as well as in less-developed nations. Examples of clinically important microbes that include Streptococcus pneumoniae, Staphylococcus aureus, Escherichia coli, Salmonella or E. coli and infections transmitted healthcare malpractices enterococci, Acinetobacter baumanii, Pseudomonas aeruginosa, and Klebsiella spp [18]. The development in the field of algal therapeutic research has made it possible by their bioactive compounds which have been found effective against most of the pathogens (Figures 1 and 2). The list of some of the algal bioactive compounds is summarized in the Table 1 [19-24].

aquaculture-research-development-antibacterial-activity

Figure 2: The antibacterial activity of chlorella vulgaris ethanol extract b) against Staphylococcus Sp. as compared with the control antibiotic streptomycin (a).

Algal species Extract source Target bacteria Reference
Pithophoraoedogonium Ethanol extract Salmonella, Staphylococcus sp., 4978 [19]
Rivulariabullata,
Nostocspongiaeforme,
Codium fragile,
ColpomeniaperegrinaSauvageau,
Cystoseirabarbata,
Zanardiniatypus
Methanol
Chloroform
Diethylether Dichloromethane Ethanol
Gram negative and Gram positive bacteria [20]
Sargassumwightii,Chaetomorphalinum, Padinagymnospora. Acetone,methonol P. aeruginosa(ATCC27853),
S. typhi-B,
Erwiniaamylovora(MTCC2760) (E. amylovora), Enterobacteraerogenes (MTCC111) (E. aerogenes), Proteus vulgaris(MTCC1771) (P. vulgaris), Klebsiellapneumonia(ATCC15380) (K. pneumonia) and E. coli(ATCC25922). gram-positive bacterial strains were Methicillin resistant S. aureus,
[21]
Asparagopsistaxiformis Ethanol extract Vibrio alginolyticus, Vibrio vulnificus and Aeromonassalmonicida subsp. salmonicidaPhotobacteriumdamselaesubsp. Damselaeand Photobacteriumdamselae subsp. piscicida, Salmonella sp., Vibrio cholerae, Vibrio harveyi and Vibrio parahaemolyticus [22]
Chlorococcumhumicola Bioactive compounds Escherichia coli, Pseudomonas aeruginosa, Salmonella typhimurium, Klebsiellapneumoniae, Vibreocholerae, Staphylococcus aureus, Bacillus subtilis, Candida albicans, Aspergillusniger and Aspergillusflavus. [23]
Gloeocapsasp. Synechocystissp. Anabaenasp. Aphanizomenonflos-aquae. Nostocsp. Nostocentophytum, Nostocmuscorum, Scytonemaocellatum, Arthrospirafusiformis(Voronich), Scenedesmusobliquus, Coelastrellasp. Chlorellasp. Rhodellaviolacea, Porphyridiumcruentum(AG.) NAG Ethanol extract Staphylococcus aureus209, Streptococcuspyogenes981, Bacilluscereus2421 Escherichia
coli3702, Pseudomonasaeruginosa1396, Salmonella
typhimurium123, and Yersiniaenterocolitica623
[24]

Table 1: Antibacterial activity of selected compounds from microalgae.

Antiviral activity of algae: The viruses have been the cause of mass epidemic and pandemic outbreaks of potentially harmful and deadly diseases like influenza, hepatitis, etc. Due to the unavailability of proper treatment facilities and precautionary measures they have been causing a great panic worldwide. Considering the present situation the discovery of antiviral compounds which were derived from algal bioactive compounds provide us a great relief. These compounds, which are tabulated in Table 2 [25-28] has a great prospective in the future.

Algal species Extract source Target Virus Reference
Haematococcus
Pluvialisand
Dunaliella
salina
Pressurized liquid
extraction
Herpes simplex
virus type 1
[25]
Gyrodinium
Impudium
(sulfated
polysaccharide,
p-KG03)
Sulfated polysaccharide Influenza virus [26]
Naviculadirecta Polysaccharide HSV1 & 2,
Influenza A virus
[27]
Gyrodiniumimpudicum p-KG03
exopolysaccharides
Encephalomyocarditis
Virus
[28]

Table 2: Antiviral activities of selected compounds from microalgae.

A number of infectious diseases caused by viruses have re-emerged in recent years, new antiviral measures are necessary for those who are not exposed to them previously. Due to this microalgae have received a strong attention to be explored for potential antiviral agents [29].

Antifungal activity of algae: The study of resistance to antifungal agents has lagged far behind that of antibacterial resistance likely because fungi were not recognized as important pathogens [30,31]. The associated increase in fungal infections prompted search for newer and safer agents to combat fungal infections [32] and a few noteworthy results encompassing microalgae are listed in Table 3 [19,24,33].

Algal species Extract source Target fungi Reference
Pithophoraoedogonium Ethanol extract Penicilliumviridicatum1101, Fusariumsolini1127 [19]
Gloeocapsa sp. Exopolysaccharides Candida albicans [24]
Haematococcuspluvialis Butanoic acid and methyl lactate Candida albicans [33]

Table 3: Antifungal activities of selected compounds from microalgae.

Antialgal activity of algae: Inhibitory phenomena between microalgal cells have been reported in the past; Bagchi et al. [34] originally proposed that natural algaecides could effectively be applied in control of toxic algal blooms like Isochrysis galbana from cell-free filtrates Dunaliella salina, Platymonas elliptica, C. vulgaris, Chaetoceros muelleri, Chlorella gracilis, Nitzschia closterium and P. tricornutum [35]. However, Pratt [36] was the first to report that growth of C. vulgaris was depressed by a compound (chlorellin) that was produced and excreted into the medium - and several other extracellular metabolites able to inhibit their own growth and the growth of other species have meanwhile been reported [37].

Antiprotozoal and Antiplasmodial activity of algae: The antiprotozoal activities algal extracts have recently been discovered against Trypanosoma brucei rhodesiense, Trypanosoma cruziand Leishmania donovaniand were found effective. The development of antiprotozoal algal extracts may prove effective in controlling various protozoan diseases and their preventive measures [38]. The crude seaweed extracts from green marine algae Cladophora rupestris, Codium fragile ssp. tomentosoides, Ulvaintestinalisand Ulva lactucahave shown anti protozoan activity against Trypanosoma brucei rhodesiense, Trypanosoma cruzi, Leishmania donovani [39]. Ciau et al.[40] studied the antiprotozoal activity of brown alga Lobophora variegataagainst Giardia intestinalis, Entamoeba histolyticaand Trichomonas vaginalis. They have extracted antiprotozoal compound by chloroform, the major compounds included -O-palmitoyl-2-O-myristoyl-3-O-(6′′′-sulfo-a-D-quinovopyranosyl)-glycerol;1,2-di-O-palmitoyl-3-O-(6′′′-sulfo-a-D-quinovopyranosyl)-glycerol and a new compound identified as 1-O-palmitoyl-2-O-oleoyl-3-O-(6′′′-sulfo-a-Dquinovopyranosyl)-glycerol [40]. The ethanolic extracts of freshwater macrophytes Potamogeton perfoliatusRanunculus tricophyllusand Cladophora glomerataas well asmarine macroalgae Dictyota dichotoma, Halopteris scoparia, Posidonia oceanica, Scinaia furcellataSargassum natansand Ulva lactucaare assayed for their in vitro antiprotozoal activity against Trypanosoma brucei rhodesiense, Trypanosoma cruzi, Leishmania donovaniand Plasmodium falciparum [41].

Trypanosomiasis is one of the most important parasitic diseases worldwide. The undesirable side effects and low efficacy of classical trypanocidal drugs underline the necessity of the development of new drugs from natural products. Although marine algae have been recognized as attractive sources of known and novel bioactive compounds, very little research has been focused on antiprotozoal activity. Aqueous and organic extracts of Rhodophyta, Phaeophyta and Chlorophyta were evaluated for their antiprotozoal activity in vitro against Trypanosoma cruzi trypomastigotes. The organic extracts from Dictyota caribea, Lobophora variegata, Turbinaria turbinata Linnaeus, and Laurencia microcladia Kützing possess promising in vitro activity against T. cruzi trypomastigotes. Laurencia microcladia is effective against Artemia salina and the high cytotoxicity exhibited by T. turbinate is required to be investigated further [42].

Red alga from genus Chondria produces cyclic polysulfides, terpenoids, amino acids and amines. Domoic acid derivatives from Chondria armata show larvicidal and blood pressure lowering activity [43]. The algal extracts have also been explores for their antiplasmodial activities, [38]. The P. falciparum (Erythrocytic stages), T. cruzi (Trypomastigotes) and L. donovani (Axenic amastigotes) are growth inhibited with the ethanol and ethyl acetate extract of algae belonging to Chlorophyta, Heterokontophyta and Rhodophyta. Antimalarial leads from marine algae, four metabolites, sargaquinoic acid, sargahydroquinoic acid, sargaquinal and fucoxanthin, were isolated from the Sargassum heterophyllum. Fucoxanthin and sargaquinal showed good antiplasmodial activity toward a chloroquine-sensitive strain of Plasmodium falciparum [44] Ethylacetate (EtOAc) extract of Sargassum swartzii and Chondria dasyphylla were investigated for larvicidal activities in larvae of malaria vector Anopheles stephensi and the mortality rate of Anopheles stephensi was 96 and 95%, respectively [45]. The endemic marine red alga Plocamium cornutum (Turner) Harvey show antiplasmodial activity in organic extracts. Interestingly, compounds bearing the 7-dichloromethyl substituent showed significantly higher antiplasmodial activity toward a chloroquine sensitive strain of Plasmodium falciparum [46].

Conclusion

We have screened the antibacterial activities of organic extracts of isolated culture of algal species and had evaluated them by agar well diffusion method. Methanol extract and ethyl acetate extract of algae were effective against few bacterial species including Staphylococcus spp. and E.coli. Methanol extracts were more effective as compared with ethyl acetate extract of algae. The antibacterial and antifungal activities were seen predominantly from the chlorella sp. as well as Chlamydomonas sp. Our work clearly summarizes the importance of microalgal extracts which have potential implication as antibacterial, antiviral, antifungal, antimicroalgal antiprotozoal as well as antiplasmodial agents. This information can prove very helpful in further research and discovery of new drugs. The work briefly explains the work carried out by various researchers, clearly elaborating the important implications of algal bioactive compounds for the application against infectious diseases and as an antimicrobial therapy.

References

  1. Tandeau-de-Marsac, HJ (1993) Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiology Reviews104:119-190.
  2. Blunt JW, Copp BR, Hu WP, Munro MH, Northcote PT, et al. (2008) Marine natural products. Nat Prod Rep25:35-94.
  3. Olaizola M (2003) Commercial development of microalgal biotechnology: from the test tube to the marketplace. BiomolEng20:459-466.
  4. Guedes AC, Amaro HM, Malcata FX (2011) Microalgae as sources of high added-value compounds—a brief review of recent work. BiotechnolProg27:597-613.
  5. Mendes RL, Nobre BP, Cardoso MT, Pereira AP, Palavra AF (2003) Supercritical carbon dioxide extraction of compounds with pharmaceutical importance from microalgae. InorganicaChimicaActa356:328-334.
  6. Mayer AMS, Hamann MT (2005) Marine pharmacology in 2001–2002: marine compounds with antihelmintic, 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. CompBiochemPhysiolC ToxicolPharmocol140:265-286.
  7. Cardozo KHM, Guaratini T, Barros MP, Falcão VR, Tonon AP, et al. (2007) Metabolites from algae with economical impact. CompBiochemPhysiol CToxicolPharmacol146:60-78.
  8. Kellan SJ, Walker JM (1989) Antibacterial activity from marine microalgae. British Journal of Phycology 23:41-44.
  9. Ozemir G, Karabay NU, Dalay MC, Pazarbasi B (2004) Antibacterial activity of volatile components and various extracts of Spirulinaplatensis. Phytother Res18:754-757.
  10. Herrero M, Ibañez E, Cifuentes A, Reglero G, Santoyo S (2006)Dunaliellasalina microalga pressurized liquid extracts as potential antimicrobials. J Food Prot69:2471-2477.
  11. Ghasemi Y, Yazdi MT, Shafiee A, Amini M, Shokravi S, et al. (2004)Parsiguine, a novel antimicrobial substance from Fischerellaambigua. Pharmaceutical Biology42:318-322.
  12. Mendiola JA, Torres CF, Martín-Alvarez PJ, Santoyo S, ToréA, et al. (2007) Use of supercritical CO2 to obtain extracts with antimicrobial activity from Chaetocerosmuelleri microalga. A correlation with their lipidic content. Eur Food Res Technol224:505-510.
  13. Metting B, Pyne JW (1986)Biologically active compounds from microalgae. Enzyme and Microbial Technology8:386-394.
  14. Salem WM, Galal H, Nasr El-deen F (2011) Screening for antibacterial activities in some marine algae from the red sea (Hurghada, Egypt). African Journal of Microbiology Research 5: 2160-2167.
  15. Tramper J, Battershill C, Brandenburg W, Burgess G, Hill R, et al. (2003) What to do in marine biotechnology? BiomolEng20:467-471.
  16. Trias J, Gordon EM (1997) Innovative approaches to novel antibacterial drug discovery. CurrOpinBiotechnol8:757-762
  17. Guedes AC, Barbosa CR, Amaro HM, Pereira CI, Malcata FX (2011)Microalgal and cyanobacterial cell extracts for use as natural antibacterial additives against food pathogens. International Journal of Food Science and Technology46:862-870.
  18. Interagency Task Force on Antimicrobial Resistance (2011) 2011 Progress Towards Implementation of: A Public Health Action Plan to Combat Antimicrobial Resistance.
  19. Danyal A, Mubeen U, Malik KA (2013) Investigating Two Native Algal Species to Determine Antibiotic Susceptibility Against some Pathogens. Curr Res J BiolSci 5: 70-74
  20. Akgul R, Suerdem TB, Akgul F (2013) Antimicrobial Activities of Some Marine Algae and Some Cyanobacteria from Canakkale J. Algal Biomass Utln 4: 35-40
  21. Rosaline XD, Sakthivelkumar S, Rajendran K, Janarthanan S (2012) Screening of selected marine algae from the coastal Tamil Nadu, South India for antibacterial activity. Asian Pacific Journal of Tropical Biomedicine S140-S146
  22. GenoveseG, Faggio C, Gugliandolo C, Torre A, Spanò A, et al. (2012) In vitro evaluation of antibacterial activity of Asparagopsistaxiformis from the Straits of Messina against pathogens relevant in aquaculture. Mar Environ Res73:1-6.
  23. Bhagavathy S,Sumathi P, Bell JS (2011) Green algae Chlorococcumhumicola-a new source of bioactive compounds with antimicrobial activity. Asian Pacific Journal of Tropical Biomedicine1:S1-S7.
  24. Najdenski HM, Gigova LG, Iliev II, Pilarski PS, Lukavsky J, et al. (2013) Antibacterial and antifungal activities of selected microalgae and cyanobacteria. International Journal of Food Science and Technology 48: 1533-1540.
  25. Santoyo S, Jaime L, Plaza M, Herrero M, Rodriguez-Meizoso I, et al. (2012) Antiviral compounds obtained from microalgae commonly used as carotenoid sources. Journal of Applied Phycology 24: 731-741.
  26. Kim M, Yim JH, Kim SY, Kim HS, Lee WG, et al. (2012) In vitro inhibition of influenza A virus infection by marine microalga-derived sulfated polysaccharide p-KG03.Antiviral Res 93:253-259.
  27. Lee JB, Hayashi K, Hirata M, Kuroda E, Suzuki E, et al. (2006) Antiviral sulfated polysaccharide from Naviculadirecta, a diatom collected from deep-sea water in Toyama Bay. BiolPharmaBull29:2135-2139.
  28. Yim JH, Kim SJ, Ahn SH, Lee CK, Rhie KT, et al. (2004) Antiviral effects of sulfated exo-polysacchride from the marine microalga Gyrodiniumimpudicumstrain KG03. Marine Biotechnol6:17-25.
  29. Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Applied Phycol7:65-68.
  30. Anaissie EJ, Bodey GP (1989) Nosocomial fungal infections - old problems and new challenges. Infectious Disease Clinics of North America3:867-882.
  31. Wey SB, Mori M, Pfaller M, Woolson RF, Wenzel RP (1988) Hospital-acquired candidemia. The attributable mortality and excess length of stay. Arch Intern Med148:2642-2645.
  32. Sánchez F, Fernández JM, Acien FG, Rueda A, Perez-Parra J, et al. (2008) Influence of culture conditions on the productivity and lutein content of the new strain Scenedesmusalmeriensis. Process Biochemistry43:398-405.
  33. Santoyo S, Rodríguez-Meizoso I, Cifuentes A, Jaime L, García-Blairsy Reina G, et al. (2009) Green processes based on the extraction with pressurized fluids to obtain potent antimicrobials from Haematococcuspluvialismicroalgae. LWT - Food Science and Technology42:1213-1218.
  34. Bagchi SN, Palod A, Chauhan VS (1990)Algicidal properties of a bloom-forming blue-green alga, Oscillatoriasp. J Basic Microbiol30:21-29.
  35. Yingying S, Changhai W, Jing C (2008) Growth inhibition of eight species of microalgae by growth inhibitor from the culture of Isochrysisgalbanaand its isolation and identification. J ApplPhycol20:315-321.
  36. Pratt R (1942) Studies on Chlorella vulgaris. V. Some properties of the growth-inhibitor formed by Chlorella cells. Amer J Bot 29:142-148.
  37. Hellebust JA (1974) Extracellular products: Algal Physiology and Biochemistry.(Stewart WDP edn),  University of California Press, Oxford, 838-863.
  38. Vonthron-Sénécheau C, Kaiser M, Devambez I, Vastel A, Mussio I, et al. (2011) Antiprotozoal Activities of Organic Extracts from French Marine Seaweeds. Mar Drugs 9:922-933.
  39. Spavieri J, Kaiser M, Casey R, Hingley-Wilson S, Lalvani A, et al. (2010) Antiprotozoal, antimycobacterial and cytotoxic potential of some british green algae. Phytother Res24:1095-1098.
  40. Cantillo-Ciau Z, Moo-Puc R,Quijano L,Freile-Pelegrín Y (2010)The Tropical Brown Alga Lobophoravariegata: A Source of Antiprotozoal Compounds. Marine Drugs8: 1292-1304.
  41. Orhan I,Sener B,Atici T,Brun R, Perozzo R,et al.(2014) Turkish freshwater and marine macrophyte extracts show in vitro antiprotozoal activity and inhibit FabI, a key enzyme of Plasmodium falciparum fatty acid biosynthesis. The Free Library.
  42. Leon-Deniz LV, Dumonteil E, Moo-Puc R, Freile-Pelegrin Y (2009)Antitrypanosomal in vitro activity of tropical marine algae extracts. Pharmaceutical Biology 47: 864-871.
  43. Afolayana AF, Boltonb JJ, Lateganc CA, Smithc PJ, Beukesa DR (2008)Fucoxanthin, TetraprenylatedToluquinone and Toluhydroquinone Metabolites from SargassumheterophyllumInhibit the in vitro Growth of the Malaria Parasite Plasmodium falciparum. Z Naturforsch C 63:848-852.
  44. Govenkar MB, Wahidulla S (2000) Constituents of Chondriaarmata. Phytochem 54: 979-81.
  45. Khanavi M, Toulabi PB, Abai MR, Sadati N, Hadjiakhoondi F, et al. (2011) Larvicidal activity of marine algae, Sargassumswartzii and Chondriadasyphylla, against malaria vector Anopheles stephensi. J Vector Borne Dis 48: 241-244.
  46. Afolayan AF, Mann MG, Lategan CA, Smith PJ, Bolton JJ, et al. (2009) Antiplasmodial halogenated monoterpenes from the marine red alga Plocamiumcornutum. Phytochemistry70:597-600.
Citation: Sanmukh S, Bruno B, Ramakrishnan U, Khairnar K, Swaminathan S, et al. (2014) Bioactive Compounds Derived from Microalgae Showing Antimicrobial Activities. J Aquac Res Development 5:224

Copyright: © 2014 Sanmukh S, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.