INTRODUCTION:

Pathogenic microorganisms consist of viruses, bacteria, protozoa, fungi and other pathogens which can cause diseases in humans. Viruses are smaller than bacteria, having sizes in the range from about 20 to 400 nm in diameter and have very unique structures. Extensive studies have been performed and treatments against these pathogens have been found yet complete eradication is still not reached. Some of the most pathogenic viruses that affect man are ZIKA virus, Human Immunodeficiency Virus (HIV), Herpes Simplex Virus (HSV), Dengue Virus (DENV), Hepatitis C Virus (HCV), Human Papilloma Virus (HPV) and their variants. These viruses multiply in the host and spread from individual to the other through contact and hence affect wide populations. Polysaccharides from algae have shown to suppress antiviral properties as well as other bioactive compounds from algae¹.

Even though there are antibiotics developed the emergence of the antibiotic resistant and multidrug resistant bacteria is a threat to public. Some of the pathogenic bacteria are the Methicillin-resistant Staphylococcus aureus (MRSA), Vancomycin-Resistant Enterococci, Drug-Resistant Streptococcus pneumonia, Drug-Resistant Mycobacterium Tuberculosis, Carbapenem-Resistant Enterobacteriaceae (CRE), MDR Pseudomonas Aeruginosa, Drug-resistant Neisseria gonorrhoeae². Protozoans are also microscopic single celled organisms and some of the diseases caused by them are malaria, sleeping sickness, Chagas disease, Leishmaniasis etc. These diseases affect people worldwide mainly in the tropical regions. The present drugs are not effective in curing them and hence novel drug compounds from seaweeds can be used for their inhibition³. Since the advancements in science and technology and methods to understand at the molecular level have increased, it has helped in discovery and development of new drugs against these pathogens⁴. Even though much research and development of medicines for various ailments are taking place in the world, the death toll by the disease-causing pathogens is very high⁵. In the United States, it has been estimated that 76 million people, annually, are victims of food diseases, resulting in five thousand deaths each year. Known pathogenic organisms cause 9.4 million infections per year, including viruses (59%), bacteria (39%), and parasites (3%)^6,7. Recently, infections have become the leading cause of death worldwide which has led to an increase in antibacterial resistance, making it a global growing problem. Thus, there is an urgent need to discover new antimicrobial compounds from plants with diverse chemical structures and novel mechanisms of action for new and re-emerging infectious diseases. The new therapeutic agents should be effective and have a novel mode of action that renders them impervious to existing resistance mechanisms⁸. The revolutionized therapy of infectious diseases by the use of antimicrobial drugs has certain limitations due to changing patterns of resistance in pathogens and side effects they produced. These limitations demand for improved pharmacokinetic properties which necessitate the continued research for new antimicrobial compounds for the development of drugs⁹. From the studies, it was noted that the standard antimicrobial drugs such as trimethoprim, fluoroquinolones, ampicillin, penicillin etc., are not efficient against drug resistant bacteria and the use of trimethoprim is not favorable^10,11. This increasing resistance of pathogenic bacteria such as vibrio cholera, Staphylococcus aureus, Salmonella sp etc. to existing antibiotics is a major problem throughout the world¹². The immedicable pathogenic virus, protozoa, fungal etc., microorganisms causing various diseases in humans is a serious threat that has to be retaliated. The ability of seaweeds to produce secondary metabolites of antimicrobial value, such as volatile components (phenols, terpenes)^13-18, steroids¹⁹, phlorotannins²⁰ and lipids¹⁹ have been already been proved. Many studies show that that different extracts from various classifications of seaweeds have showed antimicrobial properties; such as Padina sp, Galidiella sp, Laminaria sp, Enteromorpha sp to name a few²¹. Seaweeds have been explored and exploited for its various properties from thousands of years. They have been used as food, as fuel and in medicine because they produce an enormous number of secondary metabolites having various biological properties²². The research for finding the compounds which exhibit such properties and potentiality to use it in pharmaceutical industries started in the 1970s²³. Marine macroalgae are a huge reservoir of compounds possessing biological activity and a huge number of species and their novel compounds have not been explored⁵. The seaweeds have been shown to have antioprotozoal activities²⁴, hence further analysis and compound isolation will help us to discover and develop newer effective drugs. From this review, the researchers can gain insight into the antimicrobial property of the algal species and help them select seaweeds for their further studies using details of the antimicrobial properties of various seaweeds are provided.

Antiviral activity:

Viruses cause a variety of illness; while a few viruses can be treated others cause serious diseases which may result in death of a person. New compounds are highly promising since they have greater efficiency on the mutant strains of virus which are resistant to standard drugs and also show lower toxicity as they are naturally available compounds²⁵. Algae have shown to have antiviral property against various viral infections. Polysaccharides from seaweeds show antiviral property for more than 50 years²⁶. The work by Damonte in 1994 showed that the fraction F6 from the red algae Nothogeniafastigiata against Herpes Simplex Virus (HSV) type-1 with IC₅₀ 0.6 µg/mL. This fraction contained xylomannan and the fraction showed high antiviral activity against HSV-1, HSV-2, Influenza A and B virus, RSV and SIV²⁷. In the same year the aqueous extract of red seaweed A. tenera contained a galactan sulfate (GS) which inhibited the HIV-1 and HIV-2 types of viruses in MT-4 cells. As studied by Witvrouwet al., in the year 1994 they found that the galactan sulfate (GS) restricted the binding of the virus to the cells. This study showed that the GS also showed bioprotective property against Herpes virus, Arena virus, myxovirus, rhabdovirus²⁸. The extract of A. japonicus is showed anti-herpetic and viricidal activity and also concluded that a membrane was the target of interest for the compounds and Lobophora since RNA virus which lacks membrane was not affected by the extracts²⁹. Hudson continued to find antiviral property in other seaweed and hence found that the extract from C. fragile showed antiviral property against Sindbis, polio and herpes simplex virus. Other species tested were E. linza, C. bullosa, S. lomentaria and U.pinnatifida showed activity against HSV and SINV³⁰. Later in the year 2007, Mandal and his coworkers tested the fractions of C. indica containing sulphated-fucan against HSV-1 and HSV-2, by affecting the virus absorption³¹. The extraction from Hydroclathratusclathratus and Lobophora variegate gave antiherpetic results against HSV-1 and HSV-2, other strains such as acyclovir-resistant strain and moderate against activity against RSV. The compound from the fraction of H. clathratus was found to be HI-3 showing the anit-HSV property³². Rhimouet al., tested antiHSV activity in the red algae from the coast of Morocco and found that the aqueous extracts of these red algae from Morocco showed inhibitory activity against HSV-1, they are Asparagopsisarmata, Ceramium rubrum, Gelidiumpulchellum, Gelidiumspinulosum, Halopitysincurvus, Hypneamusciformis, Plocamiumcartilagineum, Boergeseniellathuyoides, Pterosiphoniacomplanata and Sphaerococcus coronopifolius³³. Another group of researchers tested the seaweed from the Brazilian coast for its antiherpetic property and they have concluded that among green algae Ulva fasciata and Codiumdecorticatum and the red algae Laurenciadendroidea containing the showed most activity against HSV-1. The green algae Penicilluscapitatus and Stypopodiumzonale showed highest activity agasint HSV-2. L. dendroidea contained Obtusol and (-)-elatol, S. zonale extract comprised of atomaric acid and these compounds accounted for the specific activity in the algae³⁴. The antiviral activity of the brown algae Sargassumnaozhouense was tested by Peng et al., in the year 2012, and polysaccharides from the algae had anti-HSV activity with EC50 value of 9.82µg/mL³⁵. First report on brown algae Lobophora variegate, has shown it to be effective against many HIV-1 strains inclusive of primary isolates and drug resistant strains. The aqueous extract also showed effectiveness in impeding viral infection to the peripheral blood mononuclear cells³⁶. Dengue is considered a dangerous health problem because there hasn’t been any active drug or treatment found against the disease. The researchers Kolshi and co-workers tested for the anti-Dengue virus (Anti-DENV) activity of eight seaweeds against the cells Huh7.5 with four serotypes of the virus and found that all the extracts were able to inhibit at least one of the types³⁷. The sulphated polysaccharide fraction of the pheophyta Cystoseiramyrica whose main component was Fucose showed effective antiviral activity against HSV and HAV³⁸. Carrageenan sulfated polysaccharide showed to inhibit the replication and propagation of the HSV-1 and RVFV. This was showed by Gomaa and his co-workers that the carrageenan sulfated polysaccharide from rhodophyta Acanthophoraspecifira and the pheophyta Hydroclathrusclathratus showed antiviral property²⁵. The polysaccharides extracted from Laurencia obtuse had highest activity among the various algae tested against the Hepatitis C virus³⁹.

Antiprotozoal activity:

Malaria is a leading cause of death due to protozoal infection. The work done by Topcu and his group showed that the novel sesquiterpene (8R*)-8-bromo-10-epi-â-snyderol was found from the chloroform-methanol extract of the red algae Laurencia obutusa showed antimalarial activity⁴⁰. Chagas disease is also a major threat to human life. The causative agent for Chagas disease is a protozoan and so they studied the efficiency of seaweeds for inhibiting the protozoa by inhibiting the dihydroorotate dehydrogenase (DHOD) enzyme. The extracts of Fucusevanescens and Pelvetiababingtoni reduced the activity of the enzyme and also the number of rate of infection in the cell⁴¹. Leishmaniasis is another disease caused by the protozoa Leishmania in humans, and is prevailing as epidemic in most of the developing countries. Hence studies were conducted on different seaweeds to test for its activity against Leishmania. The red algae Laurenciapinnatifida showed highest activity which was nearly six times more than the standard drug used for inhibiting the viability of the promastigotes stage of the protozoa⁴². Sargassumnatans showed the best trypanocidal activity against Trypanosomabruceirhodesiense, followed by Dictyotadichotoma with IC₅₀ values 7.4 mg/ml and 17.1 mg/ml respectively⁴³. The red algae Corallina officinalis and Ceramiumvirgatumshowed highest potencyagainst T. brucei rhodesiense⁴⁴. First time study was performed on the seaweeds from the northern France, Normandy coast, and it was seen that red algae Mastocarpusstellatus showed the best antiplasmodial activity with an IC₅₀ value of 2.8µg/mL⁴⁵. Another anti-Leishmanial study in the year 2011 was performed, the seaweeds from the Bushehr coast of the Persian Gulf was taken and from the results of the study it was found that the hot-water crude extract of Gracilariacorticata and Gracillariasalicornia were the strongest inhibitors among the tested algae with _IC50 of 38µg/ml and 46µg/ml respectively⁴⁶. The seaweeds collected from the Mandapam coastal area in India were collected, out of which C. peltata and C. toxifolia exhibited higher antiplasmodial activity and also lower IC₅₀ value in comparison with the standard Chloroquine⁴⁷. Dasyapedicellata collected from various coastal regions of Turkey showed high activity towards the protozoans Trypanosoma bruceirhodesiense, Trypanosoma cruzi, Leishmaniadonovani and Plasmodium falciparum with IC₅₀ values 0.37mg/mL, 62.02mg/mL, 23.04mg/mL and 0.38mg/mL respectively⁴⁸. Cystoseiratamariscifolia, C. baccataand Ulva lacthuca collected from the southern coast of England exerted highest activity against blood stage plasmodium parasites (P. berghei). U. lactuca, Ceramiumvirgatum and Halopitysincurvus showed activity against liver stage plasmodium parasites⁴⁹. Hence macroalgae can be used as a good source of antiprotozoal compounds and further research can help us discover new drugs to curb diseases caused by protozoa.

Antibacterial property:

The preliminary screening performed on the seaweeds showed that them to have antibacterial activity. The Methanol and the hexane extract of Halimeda tuna, Enhalusacoroides. Turbinariaornata, Hormophysaarticulata, Padinasp., Liaqura sp. and Sargassumsp. were active against Bacillus subtilis and Staphylococcus aureus while the methanol extract of the above mentioned algae were active against P. aeruginosa⁵⁰. The antibacterial tests conducted on some of the pathogenic organisms, the algae collected from Tanzania, Valonisaegrophila showed highest activity against S. aureus, B. subtilis and E. coli in comparison with Penicillin⁵¹. Marine algae from Southern coast of India were collected and tested, showed Rhodophyceae to highest antibacterial (Staphylococcus aureus, Vibrio spp. and Pseudomonas aeruginosa) activity than the other two classes of algae⁵². Forty four seaweeds species from the coastal regions of Canary Islands of Spain were collected and out which 28 species showed good antibacterial activity. Among these species, Asparagopsistaxiformis and Cymopoliabarbata showed activity against all the selected bacterial strains. Osmundeahybrida showed a good inhibitory activity against Mycobacterium smegmatis⁵³. The acetone extract of Caulerpacupressoides, propanol extracts of Gracilaria edulis, acetone extracts of Padinatetrastromatica and Lurenciacruciata, butanol extracts of Hypneamusciformis, Caulerpacupressoides and Chaetomorphalinoides inhibited effectively E. coli, K. pneumonia, P. aeruginosa and S. aureus respectively⁵⁴. The pathogenic bacteria Proteus mirabilis was inhibited by Gracilariacorticata and Klebsiella pneumonia was inhibited by only Stocheospermum marginatum in the study conducted on the seaweeds fromintertidal zone of Southwest coast of India¹⁸. The Vedalai coast in Tamil Nadu is a source of the green algae Codiumadherens, Ulva reticulate, Halimeda tuna were analysed for its antibacterial activity. Karthikaidevi and co-workers and they proved that the ethanol extracts of the seaweeds showed highest inhibitory activity against staphylococcus species with a zone of inhibition of 13 mm⁵⁵. The work showed that the seaweed Codiumdecorticatum showed antibacterial activity against the gram positive bacteria such as S. pneumonia, S. aureus and the gram negative bacteria E. coli, K. pneumonia, S. typhi, P. aeruginosa⁵⁶. In 2011, the ethanol extracts of Gelidiumacerosa showed high activity against the pathogens S. aureus, B. aureus. M leutus, K. pneumonia, E. coli, and P. Aeruginosa. They also analyzed that this extract had high number of secondary metabolites⁵⁷. Adaikalaraj also tested for the antibacterial activity agaisnt P aeruginosa and proved that the aqueous extract of G. verrucosa showed the highest activity⁵⁸. The compounds from the rhodophyta Laurencia obtuse were found to be 12-hydroxy isolaurene, 8,11-dihydro-12-hydroxy isolaurene, 8,11-dihydro-12-hydroxy isolaurene, all three laurene-type sesquiterpenes showed potential antibacterial activity against B. subtilis and S. aureus. Amongst the three isolauene showed the highest activity⁵⁹. Later some more compounds showed antibacterial activity such as 7-hydroxylaurene acetate, allolaurinterol acetate⁶⁰. Different extracts from the seaweeds S. wghtii, C. linum and P. gymnospora tested towards different human gram negative pathogens P. aeruginosa, S. paratyphi, E. amylovora, E. aerogenes, P vulgaris, K. pneumonia, E. coli and gram positive MRSA (Methicillin Resistant Staphylococcuus aureus), Bacillus subtilis and E. faecalis. The group proved that the acetone extract showed better activity⁵. Another work showed that the seaweeds from the Gulf of Mannar coast and showed that the ethanol extract of U. fasciata showed high activity against S. typhii, G. corticata and S. wightii towards S. flexneri showed that the seaweeds from different regions had different activities⁶¹. In 2014, a lot of work on the antibacterial inhibition by seaweeds, it was determined that the methanol was the best solvent for extraction and followed by ethyl acetate and Hexane and these showed inhibitory activity against some of the bacteria⁶². Bacteria are microscopic in structure, may be pathogenic to humans. The crude extracts of Sargassumplagyophillum, Sargassumflavellum, Padinaaustralis and Sargassumbinderi from Malaysia was extracted and showed inhibitory activity against Bacillus subtilis and Staphylococcus aureus (gram positive bacteria). The species which showed the highest inhibitory activity was the methanol extract of S. plagyophillum and showed a zone of inhibition of 12 mm against B.subtilis and the chloroform extract formed a zone of inhibition of 17 mm against B. subtilis. This proved that the seaweed S. plagyophillum has a good antimicrobial activity⁶³. The seaweeds from the red sea coast of Jeddah in Saudi Arabia were tested and it was studied that chloroform extract of the species Ulva reticulata, Caulerpaoccidentalis, Cladophorasocialis, Dictyotaciliolata, and Gracilariadendroides showed activity against Escherichia coli ATCC 25322, Pseudomonas aeruginosa ATCC 27853, Stapylococcus aureus ATCC 29213 and Enterococcus faecalis ATCC 29212 but G. dendroides>U. reticulate>D ciliolate. It was also tested that the G dendroides contained a high amount of unsaturated fatty acids abundantly the palmitic acid⁶⁴. In the same year Al-judaibi proved that T triquetra methanol extract showed growth inhibition towards S. typki, S. dysenteriae, K. pneumonia, E. aerogenes⁶⁵. According to Kannan et al., in 2014, showed that the G. corticata showed comparatively higher inhibition towards bacillus⁶⁶. In the year 2014, Kavita and group reported the first incidence of cholesterol to have antibacterial activity. The seaweed laurenciapapillosa showed high activity agasint E. coli, P. aeruginosa, K pneumonia and S. flexneri and the extract was tested for the antibacterial compound and they found that the cholesterol compound was found to be 24-propylidene cholest-5-en-3-ol⁶⁷. Listeria monocytogenes is a food-borne pathogen and so lee and his coworkers worked towards finding antibacterial agents. From their work, it was found that the chloroform fraction of the brown alga Myagropsismyagroides showed strong inhibitory activity against L. monocytogenes and Clostridium Perferinges and that the cytoplasmic membrane of the bacteria was targeted⁶⁸. Another work by Yuvraj and Arul reported that methanol extract from G. salicomia and A. hydrophila from the Qesham island coast, showed a high inhibitory rate against gram negative rod-shaped bacterium⁶⁹.

Antifungal property:

There are many fungal pathogens found to infect humans such as Aspergillus flavus, Aspergillus niger, Aspergillus fumigatus, C. albicans, C. tropicalis. Many researchers have tried to find a way to inhibit these microorganisms and since seaweeds have shown to have multiple valuable properties, they have been tested and shown to exhibit antifungal property as well. Elsie and his co-workers thus tested the extracts of G. acerosa against the pathogenic fungi and their work confirmed that the ethanol extract of the seaweed showed high anti-fungal activity against Aspergillus species (A. flavus, A. nigerand A. fumigatus) and the Candida species (C. albicans, C. tropicalis)⁵⁷. This was an important step towards finding novel compounds against pathogenic fungi. Later onAlarif found that the Isolaurene from Laurencia obtuse against C. albicans⁵⁹. Another study proved that the novel compound symphyocladin G which is a bromophenol-urea adducts exhibited inhibitory activity against C. albicans⁷⁰. A study by Pandithurai et al., 2015, showed that highest inhibition of Candida albicans, Candida tropicalis, Trichophyton mentagrophytes was seen by methanolic extract and inhibition of Aspergillus flavus was seen by chloroform extract of S. asperum respectively⁷¹. The methanolic extract of Ulva rigidacollected from the Arzew gulf of Algeria’s western coast showed activity against pathogenic fungi Candida albicans, Aspergillus niger and Cryptococcus neoformans^72-74. The Ulva lactuca collected from the western coastal region of India at the Okha coast was tested to have strongest inhibition towards Aspergillus niger⁷⁵. In the same year the brown algae from Moroccan Atlantic coast showed activity against four Candida sp⁷⁶. The Gracilaria edulis was collected by Aswathi and Jamila in 2014, from coast of Tuticorin at the Gulf of Mannar. The acetone extract had good inhibition against A. terreus and F semitectum⁷⁷.

CONCLUSION:

This review shows the antipathogenic property of the algal extracts from different regions of the world. The pathogenic organisms cause a varied list of diseases and result in damage to organs in humans. The large number of secondary metabolites present in the seaweeds have garnered its value in food, fuel and medicine. Due to its multiple properties researchers were interested to find out if they have antimicrobial properties against the various human pathogens and thus seaweeds have excelled in their array of functions as they have proven to have antimicrobial properties as well. So, the research in this field has led to identification of seaweeds having such properties from different regions around the globe. In this review, we have listed out the work done until now to find potential drugs for numerous human pathogens from different places. Most of the work have revealed only the extracts showing the activities, and hence further investigation and phytochemical studies into these extracts can reveal the important compounds presenting the antipathogenic property. These compounds can be a potential drug for inhibiting the growth of the pathogens, the replication of the pathogen within the body, inhibiting infection itself by showing minimal harmful effects on the human cells and health or an efficient candidate for the drug-resistant pathogens. In the future studies, researchers can use this information to investigate the major class of compounds in the particular extract or the main component in with the inhibitory property in the seaweeds mentioned in this review.

ACKNOWLEDGEMENT:

The authors gratefully acknowledge VIT University, Vellore for the support through Seed Grant for Research.

CONFLICT OF INTEREST:

The authors declare no conflict of interest.

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Received on 28.06.2017 Modified on 10.08.2017

Research J. Pharm. and Tech 2018; 11(9): 3957-3963.

DOI: 10.5958/0974-360X.2018.00727.8