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Marine Algicolous Endophytic Fungi J. Microbiol. Biotechnol. (2017), 27(6), 1039–1052 https://doi.org/10.4014/jmb.1701.01036 Research Article Review jmb Marine Algicolous Endophytic Fungi - A Promising Drug Resource of the Era S Manomi Sarasan1†, Jayesh Puthumana2†, Neema Job1, Jeonghoon Han2, Jae-Seong Lee2*, and Rosamma Philip1* 1Department of Marine Biology, Microbiology, and Biochemistry, School of Marine Sciences, Cochin University of Science and Technology, Kochi-682016, Kerala, India 2Department of Biological Science, College of Science, Sungkyunkwan University, Suwon 16419, Republic of Korea Received: January 13, 2017 Revised: April 2, 2017 Endophytic fungi have currently been acknowledged as the most promising source of Accepted: April 3, 2017 bioactive compounds for drug discovery, and considerable progress has been made in First published online exploring their diversity, species richness, and bioprospecting. Fungal endophytes from April 5, 2017 unique environmental settings offer a pool of potentially useful medicinal entities. Owing to *Corresponding authors the constant stresses imposed on macroalgae by marine environments, it is believed that algae R.P. and their associated endophytic symbionts represent a good source of structurally diverse Phone: +91-484-236-8120; E-mail: [email protected] bioactive secondary metabolites. Despite the proven significance of active metabolites of algal J.-S.L. endophytes, little have been exploited. This review highlights the latest discoveries in Phone: +82-31-290-7011; algicolous endophytic research, with particular focus on the bioactive metabolites from algal E-mail: [email protected] endophytes. Compounds are classified according to their reported biological activities, like † These authors contributed anticancer, antibacterial, antifungal, and antioxidant properties. Present experimental equally to this work. evidence suggests that a majority of the bioactive metabolites were reported from S upplementary data for this Phaeophyceae followed by Rhodophyceae and Chlorophyceae. An intensive search for newer paper are available on-line only at http://jmb.or.kr. and more effective bioactive metabolites has generated a treasure trove of publications, and this review partially covers the literature published up to 2016. pISSN 1017-7825, eISSN 1738-8872 Copyright© 2017 by Keywords: Macroalgae, endophytic fungi, secondary metabolite, bioactive compound, The Korean Society for Microbiology anticancer, antimicrobial and Biotechnology Introduction and archaebacteria, and the most frequently observed candidates might be “mycoendophytes” [4]. To date, most In one of the primal articles regarding endophytism, reviews have focused on highly diverse, polyphyletic Petrini [1] stated these were all organisms inhabiting plant assemblages of endophytic ascomycetous fungi, with organs that at some time in their life can colonize internal plant Aspergillus sp. as the dominant taxa [3, 8]. tissue without causing apparent harm to the host. They cause Fungal endophytes have profound effects on stimulation no overt tissue damage hence producing no symptoms, of plant growth, increased disease resistance, improvement and in fact, there exists no evidence for even their presence of the plant’s ability to withstand environmental stresses, in plants [2]. Collectively, the fungal survey of various and recycling of nutrients [9]. Besides these, endophytes hosts have suggested the ubiquity of endophytes and may possibly produce a surfeit of bioactive metabolites as revealed their symbiotic association in all healthy plant the outcome of an intimate relationship with the host, and taxa studied to date, typically more than one guest in each may serve as potential sources of novel natural products flora [3, 4]. Being non-organ-specific, endophytes invade for exploitation in medicine, agriculture, and industry [10]. all organs and reside entirely within plant tissues beneath Several studies do indicate that the active principle of the epidermal cells, intracellularly or intercellularly [5-7]. fungal endophytes expresses more activity than those of In general, endophytes include fungi, bacteria, mycoplasma, their respective hosts [2]. A diverse array of novel, eco- June 2017 ⎪ Vol. 27⎪ No. 6 1040 Sarasan et al. friendly secondary metabolites comprising bioactivities (anticancer, antioxidant, antifungal, antibacterial, antiviral, anti-insecticidal, and immunosuppressant) have been procured from endophytes [11]. The role of endophytes in drug discovery began in the 90s with the isolation of taxol, world’s first billion dollar anticancer drug, and led to an explosion in endophytic studies [12]. Endophytes have also been investigated for their roles in agriculture and biofuel production. Inoculating crop plants with certain endophytes may provide increased disease or parasite resistance, thus improving food production to fulfill the needs of increasing populations. Some endophytes have been proved to possess metabolic processes that convert cellulose and other carbon sources into “myco-diesel” and other hydrocarbon derivatives [13]. Herein, we review the biopharmaceutical compounds explored from marine algal endophytes and briefly discuss the myco-phyco interactions, isolation techniques, and bioprospecting. Fig. 1. Asymptomatic colonization of endophytes. Algicolous Endophytes A balanced antagonism between endophytic virulence and plant defense results in effective colonization of endophytes. In the marine realm, macroalgae offer a wide range of therapeutic possibilities and have been widely exploited in traditional and folk medicine for more than 2,000 years in fungal partner trades secondary metabolites (conferring China as well as ancient Egypt. It seems obvious that algae- stress tolerance) for nutrition and self-defense with algae derived compounds have antimicrobial and antifouling [2, 20, 21], whereas commensalism benefits the microbial activities and are hence used in cosmetics or antifouling partner only [22]. Under certain rare conditions, the paints [14]. It is relevant to consider that the secondary endophyte may become parasitic and cause disease in the metabolites that a fungus synthesizes may correspond with host [23, 24]. Schulz and Boyle [19] proposed a hypothesis its respective ecological niche, and continual metabolic of balanced antagonism between endophytic virulence and interactions between the fungus and plant may enhance the host defense, resulting in asymptomatic colonization synthesis of these metabolites [15]. Because of the presence (Fig. 1). Interestingly, endophytes retain almost the same of a constant, inexorable stress foisted on macroalgae virulence factors as that of pathogens, and produce several (prolonged periods of sunlight exposure, sharp variation in exoenzymes resulting in host colonization [16, 25], whereas moisture and salt concentration, changing tides, abundant the host can respond by activating its defense mechanism microorganisms and herbivore insects), it seems more as it would to a pathogen. As long as endophytic virulence likely that algae and their endophytic symbionts would be and host defense maintain balance, the interaction remains a good source of biologically active secondary metabolites symptomless. Any kind of imbalance due to any kind of [16]. Even though algae represent the second largest source stress in the host leads to mortality of endophytes by host of marine fungi after mangrove swamps [17], most of the defense or a disease condition in the host by endophyte tropical and subtropical algal species have been scarcely virulence. The balance of antagonism appears to be often assessed for endophytic assemblages, whereas research has plastic, depending on environmental factors and nutritional been progressing in temperate regions [18]. status, as well as the developmental stages of partners [19]. While considering the nature of the interaction, it is important to think of the complexity of their relationship in Isolation of Endophytes from Macroalgae great detail. Schulz and Boyle [19] recognized three types of host-endophyte interactions, ranging from mutualism It is essential to understand the methods and rationale through commensalism to parasitism. The most common used to isolate most potent endophytes from various type of myco-phyco interaction is mutualism, in which the ecological niches. Isolation of endophytes should be accurate J. Microbiol. Biotechnol. Bioactive Compounds from Algal Endophytes 1041 enough to eliminate epiphytic microbes that reside on the sequences available in the GenBank database [33]. algal surface. Algal samples for isolation purpose should look apparently healthy and disease free in order to Biopharmaceutical Compounds from Algal minimize the presence of pathogenic and saprobic species, Endophytes and to avoid isolation of localized pathogenic endophytic microorganisms [4, 10]. Care should be taken to process the The grand entry of taxol, the world’s first billion dollar samples as quickly as possible following collection, to anticancer drug, had augmented the importance of evade contamination by air microspores [26], or be kept at endophytes and shifted natural product research to 4°C until analysis in the case of any inconvenience [12]. endophytic fungi. The discovery of anticancer drug taxol One major challenge in the isolation of endophytic taxa is was from the yew tree Taxus brevifolia in the 70s [34]. The surface sterilization, which varies according to the species view of Stierle et al. [35] was that yew trees might support as well as tissue type
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