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ORIGINAL ARTICLE

Screening of antimicrobial activity of macroalgae extracts from the Moroccan Atlantic coast Criblage de l’activité antimicrobienne des extraits des macroalgues des côtes atlantiques marocaines M. El Wahidi a, B. El Amraoui a,b,∗, M. El Amraoui a, T. Bamhaoud a a

Laboratoire contrôle qualité en bio-industrie et molécules bio-actives, faculté des sciences, université Chouaib Doukkali, BP 20, 24000 El-Jadida, Morocco b Faculté polydisciplinaire de Taroudant, université Ibn Zohr, BP 271, 83000 Taroudant, Morocco Received 25 October 2014; accepted 17 December 2014

KEYWORDS Macroalgae; Candida; Antibacterial activity; Antifungal activity; Cryptococcus



Summary The aim of this work is the screening of the antimicrobial activity of seaweed extracts against pathogenic bacteria and yeasts. The antimicrobial activity of the dichloromethane and ethanol extracts of ten marine macroalgae collected from the Moroccan’s Atlantic coast (El-Jadida) was tested against two Gram+ (Bacillus subtilis and Staphylococcus aureus) and two Gram− (Escherichia coli and Pseudomonas aeruginosa) human pathogenic bacteria, and against two pathogenic yeasts (Candida albicans and Cryptococcus neoformans) using the agar disk-diffusion method. Seven algae (70%) of ten seaweeds are active against at least one pathogenic microorganisms studied. Five (50%) are active against the two studied yeast with an inhibition diameter greater than 15 mm for Cystoseira brachycarpa. Six (60%) seaweeds are active against at least one studied bacteria with five (50%) algae exhibiting antibacterial inhibition diameter greater than 15 mm. Cystoseira brachycarpa, Cystoseira compressa, Fucus vesiculosus, and Gelidium sesquipedale have a better antimicrobial activity with a broad spectrum antimicrobial and are a potential source of antimicrobial compounds and can be subject of isolation of the natural antimicrobials. © 2015 Published by Elsevier Masson SAS.

Corresponding author. E-mail address: [email protected] (B. El Amraoui).

http://dx.doi.org/10.1016/j.pharma.2014.12.005 0003-4509/© 2015 Published by Elsevier Masson SAS.

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MOTS CLÉS Macroalgues ; Candida ; Activité antibactérienne ; Activité antifongique ; Cryptococcus

Résumé L’objectif de ce travail est le criblage de l’activité antimicrobienne des extraits d’algues marines contre des bactéries et des levures pathogènes. L’activité antimicrobienne des extraits organiques et hydroalcooliques de dix macroalgues récoltées des côtes atlantiques marocaines (El-Jadida) a été effectuée contre deux bactéries Gram positif (Bacillus subtilis et Staphylococcus aureus), deux bactéries Gram négatif (Escherichia coli et Pseudomonas aeruginosa) et deux levures pathogènes (Candida albicans et Cryptococcus neoformans) par la méthode de diffusion à partir des disques de cellulose. Parmi les dix algues étudiées, sept (70 %) ont montré une activité contre au moins un microorganisme pathogène étudié, cinq (50 %) sont actifs contre les deux levures étudiées avec un diamètre d’inhibition supérieur à 15 mm pour Cystoseira brachycarpa, six (60 %) algues présentent une activité antibactérienne dont cinq (50 %) présentent un diamètre d’inhibition antibactérien supérieur à 15 mm. Les algues brunes, Cystoseira brachycarpa, Cystoseira compressa et Fucus vesiculosus et l’algue rouge, Gelidium sesquipedale ont montré une forte activité antimicrobienne avec un large spectre antimicrobien et peuvent être une source potentielle de composés antimicrobiens et peuvent faire l’objet de l’isolement d’agents antimicrobiens naturels. © 2015 Publi´ e par Elsevier Masson SAS.

Introduction With severe fungal infections, responsible for a high mortality rate among immunosuppressed patients (cancer, AIDS, transplantation) and the emergence of new bacterial strains resistant to current antibiotics, the search of a new antimicrobial from natural source became an obligation. Lower marine organisms are one of the richest sources of both biologically active secondary metabolites and chemical diversity [1,2]. These natural products have as important role in repulsion of predators [3,4] and pathogen organisms. Algae are found in all seas, at all latitudes and to record depths of 268 m (Bahamas) [5]. The algae are also used for their nutrition, fertilizers and therapeutic properties. In Morocco, the use of seaweed from the Atlantic coast began in the mid 20th century by exploiting Gelidium for the production of agar. Marine algae have been widely used as biological material in Moroccan laboratories [6,7] and were the source of many biological molecules [8—11]. However, the chemistry of marine algae of the Moroccan coast is still undefined. In this report, we describe the biological effect activity of dichloromethane and ethanol extracts of ten marine algae collected from the Moroccan Atlantic coasts for their antimicrobial activities against four human pathogenic bacteria and two human pathogenic yeasts in order to find new potent antimicrobial metabolites with a broad spectrum antibiotic.

Materials and methods Biological materials Two green algae, three red algae and five brown algae were collected from three difference sites in the Atlantic coast of El-Jadida province, Morocco. After sampling, seaweeds were cleaned, washed with sea water and immediately

transported to the laboratory to be washed with distilled water. Algae species and their sampling sites are reported in Table 1 and the geographical localisation of these sampling sites is shown in Fig. 1.

Preparation of the seaweed extracts Each alga (100 g of crushed fresh algae) was ground and extracted with absolute ethanol (3 × 300 mL) with stirring in a dark chamber for 48 h and filtered. The filtrates were combined and evaporated at reduced pressure until total evaporation of ethanol. The suspension is completed with distilled water to 100 ml as final volume and extracted with CH2 Cl2 (3 × 100 ml). The CH2 Cl2 extracts were combined, dried on anhydrous sodium sulphate (Na2 SO4 ), filtered and concentrated at reduced pressure to give a dichloromethane extract (extract C).

Table 1 Algae specie and their sampling sites. Espèces d’algues et leur site de récolte. Algae class

Algae specie

Sampling site

Chlorophyceae

Ulva lactuca Codium fragile

1 3

Rhodophyceae

Gelidium sesquipedale Gelidium attenuatum Chondrus crispus

3 3 3

Pheophyceae

Bifurcaria bifurcata Fucus vesiculosus Laminaria ochroleuca Cystoseira compressa Cystoseira brachycarpa

3 1 2 3 3

The geographical location of sampling sites are shown in Fig. 1.

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Figure 1. Geographical localisation of sampling sites of seaweeds. Localisation géographique des sites de récolte des algues marines

The aqueous phases were lyophilised and twice dissolved in absolute ethanol, then filtered and concentrated at reduced pressure to give a ethanol extract (extract B). The extracts (B and C) were tested for their antimicrobial activities.

bacteria or 28 ◦ C for fungi. Inhibition zones were measured after 24 h of incubation. Standard disks of the antibiotic rifampicine (30 ␮g) and nystatin (100 ␮g) served respectively as the positive antibacterial and antifungal controls. All tests were performed in triplicate.

Microorganisms and media Four bacteria and two fungal species obtained from the fungi culture collection (FCC) of the National Cultures Collection of Microorganisms of the Pasteur Institute, Paris, France, from the Collection of Pasteur Institute (CIP), and from the American Type Culture Collection (ATCC) were used as the antimicrobial test strains: Bacillus subtilis ATCC66331, Escherichia coli CIP54127, Staphylococcus aureus CIP209, Pseudomonas aeruginosa ATCC10145, Candida albicans CIP884.65, Cryptococcus neoformans ATCC 11576. The bacterial strains were maintained on the Luria Bertani and yeast on the Sabouraud’s agar medium [12].

Agar disk-diffusion assay The screening of antimicrobial activity of the marine algae extracts was carried out with agar disk-diffusion method [13] using Muller Hinton Agar (MHA) medium [Difco] for antibacterial activity and yeast morphological agar (YMA) medium [Difco] for antifungal activity. The bacterial and yeast inocula were prepared by suspending in 9 mL of sterile water the colonies from 24 h culture on Luria Bertani and Sabouraud’s agar medium, respectively. The cell density was determined by a hemocytometer and adjusted to 104 UFC/ml for the yeast and 106 UFC/ml for the bacteria. Each disk containing 500 ␮g of algae crude extract was applied on the test media previously inoculated with each test strain. Plates were kept at 4 ◦ C for at least 2 h to allow the diffusion of chemicals, and then incubated at 37 ◦ C for

Results and discussion The results of antibacterial and antifungal activities of the marine algae extracts against pathogenic bacteria and fungi are summarized in Tables 2 and 3 respectively. Among the algae: • seven algae (70%) are active against at least one pathogenic microorganisms studied; • five (50%) are active against the two studied yeast with an inhibition diameter greater than 15 mm for Cystoseira brachycarpa; • six (60%) are active against at least one studied bacteria with five (50%) algae exhibit antibacterial inhibition diameter greater than 15 mm. Antibacterial and/or antifungal activities depend on the algae family.

Pheophyceae (Brown algae) Laminaria ochroleuca is the only brown algae of this class witch didn’t show any antimicrobial activity. Fucus vesiculosus is only active against Gram positif bacteria, while and the extracts of Cystoseira genus are active against all pathogenic bacteria and yeasts studied with inhibition diameter greater than 15 mm. The ethanolic extract of Bifurcaria bifurcata is active against all bacterial and fungal strains studied while the dichloromethane extract is only active against Gram-positive bacteria with an inhibition diameter greater than 10 mm. The biological

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M. El Wahidi et al. Table 2 Screening of antibacterial activity of marine algae extracts. Criblage de l’activité antibactérienne des extraits d’algues. Seaweed

Extract(500 ␮g)

Gram-negative bacteria

Gram-positive bacteria

Escherichia coli CIP54127

Pseudomonas aeruginosa ATCC10145

Staphylococcus aureus CIP209

Bacillus subtilis ATCC66331

Bifurcaria bifurcata

B C

+ —

++ —

+++ ++

++ +

Fucus vesiculosus

B C

— —

— —

+ +++

+ +++

Laminaria ochroleuca

B C

— —

— —

— —

— —

Cystoseira compressa

B C

+++ —

+++ —

+++ —

+++ —

Cystoseira brachycarpa

B C

++++ —

++++ —

++++ —

++++ —

Gelidium Sesquipedale

B C

+++ —

+++ —

+++ +

+++ —

Gelidium attenuatum

B C

++ —

++ —

++ —

++ —

Chondrus crispus

B C

— —

— —

— —

— —

Codium fragile

B C

— —

— —

— —

— —

Ulva lactuca

B C

— —

— —

— —

— —

Rifampicine 30 ␮g

++++

++++

++++

++++

—: no activity; +: inhibition diameter < 10 mm; ++: inhibition diameter < 15 mm; +++: inhibition diameter < 20 mm; ++++: inhibition diameter > 20 mm; B: ethanol extract; C: dichloromethane extract; 500 ␮g/disk.

activities of brown algae are confirmed by several studies [14—18].

Rhodophyceae (red algae) Extracts of the Gelidium genus have antifungal and antibacterial activity against all pathogenic bacteria and fungi while Chondrus cripus is not active against any pathogenic bacterial or fungal strain.

Chlorophyceae (green algae) In this study, Codium fragile and Ulva lactuca extracts aren’t active against bacteria and pathogenic yeasts studied. However, several studies have demonstrated the richness of these two algae with different biological compounds [19—26]. Marine organisms have been widely used as biological material in the research of a new biomolecules. Seaweeds having a very important role in the marine environment have been studied because they are abundant and easily accessible. Different biological activities of extracts have been reported and approved by several works [6,9,11,27].

However, given the large number of algae still unaccounted for and the geographic and seasonal variations of the secondary metabolism of certain algae, research of new products still continues. Moroccan marine coasts are rich in marine life, many research laboratories have studied and still studying the use of marine algae in several domains, including the isolation of biomolecules [7,28—31], extracting agar [32] and other functions [33—39]. Marine coast of El-Jadida is very rich in marine algae and is known by harvesting the red alga, G. sesquipedale [40]. The province of El-Jadida concentrates more than 80% of the national production of this alga prized for its rich agar. Forty percent of the harvest is exported while the remainder is converted into natural gelling agent, used particularly for the preparation of jams or cosmetics. Algae are less evolved organisms without physical defence, living in severe environmental and ecological conditions (pressure, salinity, lack of light, inter-and intraspecific skills. . .). So, these organisms produce their own chemical defences. These so-called, secondary metabolites are biologically active molecules and high structural originality. Many studies have focused on the identification of

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Table 3 Screening of antifungal activity of marine algae extracts. Criblage de l’activité antifongique des extraits d’algues. Marine algae species

Extract (500 ␮g)

Candida albicans CIP884.65

Cryptococcus neoformans ATCC 11576

Bifurcaria bifurcata

B C

++ —

++ —

Fucus vesiculosus

B C

— —

— —

Laminaria ochroleuca

B C

— —

— —

Cystoseira compressa

B C

++ ++

++ ++

Cystoseira brachycarpa

B C

+++ —

+++ —

Gelidium Sesquipedale

B C

— ++

— ++

Gelidium attenuatum

B C

+ —

++ —

Chondrus crispus

B C

— —

— —

Codium fragile

B C

— —

— —

Ulva lactuca

B C

— —

— —

Nystatine 100 ␮g

++++

++++

—: no activity; +: inhibition diameter < 10 mm; ++: inhibition diameter < 15 mm; +++: inhibition diameter < 20 mm; ++++: inhibition diameter > 20 mm; B: ethanol extract; C: dichloromethane extract; 500 ␮g/disk.

several biological or pharmacological activities of these molecules as the antibacterial effect [41], antiviral [42—44], antifungal [45,46], antifouling [47,48] and cytotoxic [49,50]. The Cystoseira genus is widely studied for its chemical composition and biological activities [15—18,36,51]. Most of the secondary metabolites produced by seaweeds have bacteriocidal or the antimicrobial compounds derived from seaweeds consist of diverse groups of bacteriostatic properties brominates phenols, oxygen heterocyclic; terpenols, sterols, polysaccharides, dibutenolides peptides and proteins [52].

Conclusion Preliminary results showed that different species of algae have an antibacterial or antifungal potential. Thus, the Moroccan algae constitute a potential source of new compounds can be used in the field of health. The phyophiceae and rhodophyceae are classes of algae that exhibit antimicrobial activity. Brown algae, C. brachycarpa, C. compressa and F. vesiculosus, and read alga G. sesquipedale have a better antimicrobial activity with a broad spectrum antimicrobial and are a potential source of antimicrobial compounds and can be subject for isolation of the natural antimicrobials.

Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.

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Screening of antimicrobial activity of macroalgae extracts from the Moroccan Atlantic coast.

The aim of this work is the screening of the antimicrobial activity of seaweed extracts against pathogenic bacteria and yeasts. The antimicrobial acti...
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