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Mangrove Plants as a Source of Bioactive Compounds: A Review

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Mangrove plants as a source of bioactive compounds: A review

Nilesh Lakshman Dahibhate, Ankush Ashok Saddhe, Kundan Kumar*

Department of Biological Sciences, Birla Institute of Technology and Science Pilani, K. K.

Birla Goa Campus, Sancoale, Goa 403726, India

* Corresponding author

Kundan Kumar, Ph.D.

Assistant Professor

Department of Biological Sciences

Birla Institute of Technology & Science

K.K. Birla Goa Campus, Goa-403726, India

Tel: 91-832-2580196

Email: [email protected]
Abstract

Mangroves are unique coastal forest ecosystem distributed along the tropical and subtropical

region of the world. They are evolutionarily adapted to combat against hostile environmental

conditions such as low oxygen, high salinity, and temperature. The adaptive features

endowed with novel secondary metabolic pathways and bioactive compounds to sustain in

harsh conditions. The novel metabolites are rich source of the wide range of bioactive

compounds and natural products. It includes terpenoids, alkaloids, phenolics, saponins,

flavonoids, and steroids. The bioactive and natural compounds may serve as therapeutic

precursors and industrial raw materials. Terpenes and polyphenols have antiviral,

antibacterial, antifungal, antimalarial, anticancer or combination of activities. To date, several

mangroves plants were examined and recognized as a potential source of novel natural

product for exploitation in medicine. In fact, most of isolated compounds are novel and

showed promising biological activities such as gastroprotective, cytotoxic, antioxidant,

antibacterial, antifungal, antiviral, enzyme activation and inhibition, immunosuppressive,

anti-inflammatory, antifeedant effects. In the present review, we have compiled the

achievements and progress in mangroves natural products research of the last decade.

Keywords: Mangrove, Bioactive, Terpenoids, Alkaloids, Secondary metabolites.

1. Introduction

Mangroves are a rich source of secondary metabolites having wide applications in pharmacy

and medicine. Mangroves are coastal ecosystems, sheltered at estuaries and along the river

banks and the lagoons in the tropic and subtropic areas of the world [1-2]. Mangroves are

evolutionarily adapted to combat against hostile environmental conditions such as low

oxygen, high salinity, and temperature. These unique adaptive features and evolved

secondary metabolic pathways may be responsible for the synthesis of structurally diverse

metabolites to sustain mangroves in extreme conditions. These metabolites are function as the

source of a wide range of bioactivities and plays important role in defense and survival. The

most important bioactive compounds belong to three structural classes such as nitrogen

containing (alkaloids and amines), terpenoids and phenolic (phenolic acids, tannins,

flavonoids, quinones) compounds [3-4].

Mangroves are the diverse source of bioactive metabolites such as essential oils [5],

limonoids [6], flavonoids [7], coumarins [8], terpenoids [9-10], glycosides [11] and alkaloids

[12]. There are 73 mangrove species distributed in 123 countries of the world [13] with

economic and traditional folkloric medicinal value. They are used for the treatment of

dyspepsia, hepatitis, asthma, diabetes, leukemia, stomach problems, antibacterial, antiherpetic

and anthelmintic [14-16]. They are also effective in the treatment of malaria and syphilis

[17]. Mangroves species have a piscicidal and gastroprotective effect [18]. Moreover,

antioxidant [19], anticancer [20-21] and anti-inflammatory [22] activities of the extract of

mangroves species have been widely reported.

The crude extracts of most mangroves species have been reported to display inhibitory

activity against several microorganisms and cancerous cell lines [23] However, the bioactive

compounds responsible for most of these activities have not yet been isolated. In recent years,
there has been considerable interest in the phytochemistry and medicinal properties of

mangroves species [24-25].

This review has been set out to compile the research in last decades on a novel compounds

from mangroves which show promising biological activities. In the present review, we have

compiled the recent achievements and progress in mangroves bioactive compound research.

2. Biological activities

Mangroves species have various applications in folk medicine. Extracts from these plants are

of great importance because of the synthesis of diverse metabolites to cope with the harsh

condition. The efficacy of mangrove extracts as anticancer as well as antimicrobial agents

have been widely reported. There are different types of mechanism of action postulated for

the plant secondary metabolites which can interfere and target pathogen metabolic process

and signal transduction pathway or alter the gene expressions [26]. In the current review, we

have mainly focused on the mangrove bioactive compounds having anticancer, antimicrobial,

anti-inflammatory and antioxidant activity. The list of biological properties of mangrove

derived bioactive compounds mentioned in Table 1.

2.1 Anticancer activity of isolated novel compounds

Cancer is a leading cause of death. Plant derived bioactive compounds have promising

anticancer activity [27] and some of them can be used as a potential drug against breast

cancer [28]. Novel anticancer compounds were isolated and characterized from different

mangroves species such as Aegiceras corniculatum, Excoecaria agallocha, Rhizophora

stylosa, Sonneratia paracaseolaris, Xylocarpus genus, Ceriops tagal, and Bruguiera

cylindrica. New triterpene, saponins, aegicoroside A (1) were isolated from the leaves of A.

corniculatum. It has been reported to inhibit the growth of human cancer cell line such as
MCF7, HCT116, B16F10 and A549 [29]. Extraction of twigs and leaves of the mangrove

plant E. agallocha from Vietnam yielded two new beyerene-type diterpenoids namely

Excoecarin L (2) and Excoecarin O (3). They were tested for cytotoxic activity against two

human cancer cell lines KB and LU-1 but both the compound showed weak activities [30]. A

new bioactive cycloartane glucoside named as rhizostyloside (4) present in R. stylosa

demonstrated cytotoxicity against human cancer cell line such as, KB, LU-1, SK-Mel-2 and

reported its role in the activation of caspase 3/7 in LU-1 cell line [11]. A chemical

investigation of the aerial part of S. paracaseolaris showed a presence of five new

triterpenoids, paracaseolins A-E (5-9) compounds [31]. They were evaluated for activities

against the selected P388, HeLa, A549, and K562 tumor cell lines. The compound

paracaseolin D shows potent cytotoxic activity against A549 cell line whereas paracaseolin A

exhibited significant anti-H1N1 virus activity. Naturally limonoids are present as highly

oxidized tetranortriterpenoids and prevalently found in Meliaceae and Rutaceae family

member [32]. The Xylocarpus genus is known to produce a variety of limonoids, especially

mexicanolides and phragmalins. There are several medicinally important limonoids were

reported from seeds of X. granatum such as limonoids named thaixylogranins A-H (10-17).

All the isolated compounds exhibited weak cytotoxicity against the MDA-MB-231 cell line

[33]. Furthermore, previously unreported seven new apotirucallane protolimonoids isolated

from the twigs and leaves of X. granatum namely, xylogranatumines A-G (18-24). Among

the isolated compounds the xylogranatumine F, is found to exhibit in vitro cytotoxic activity

against A549 cells [34]. Similarly, four novel tetranortriterpenoids, xylomexicanins E-H (25-

28), were isolated and showed that xylomexicanin E is the first example of limonoid with

azaspiro skeleton between B and C rings. Xylomexicanin E showed moderate activity against

the cell line A 549 and RERF [35]. C. tagal with high medicinal value and two new

phenylpropanoids named as tagalphenylpropinoidin A (29) and tagalphenylpropinoidin B

(30), were isolated from its stem and twig. The anti-tumor activities of two compounds were

evaluated against MCF-7 and HL-60 cell line and also showed that high methylation altered

its anti-tumor activity [36]. In addition, two new dolabranediterpenes namely tagalenes J (31)

and K (32) were isolated. They were checked for cytotoxic activity against MCF-7, SW480,

HepG2, HeLa, PANC-1 and A2058 cell lines [37]. Recently, four new diterpenes named

tagalons A-D (33-36) belongs to isopimarane (A) two 16-nor-pimaranes (B-C), and dolabrane

(D) type were isolated from the C. tagal. Most notably, tagalons C and D exhibited selective

cytotoxicity against the human breast cancer MT-1 cell line [38]. Moreover, a new dolabrane

dinorditerpene, tagalsine X (37) was isolated from the leaves of C. tagal and evaluated for

cytotoxic activities against four human carcinoma cell lines, CNE-2, HCT-116, HepG2 and

A549 respectively. Tagalsine X showed no obvious inhibitory activity against the above four

tested cancer cells [39]. However, the direct utilization of mangrove materials for medicine

production will likely reduce mangrove resources. A better way for this application is to

formulate new medicines through chemical synthesis based on the compound configurations

of related compounds found in certain mangrove materials. A β-Taraxeryl-trans-p-

chlorocinnamate (38), a chemically transformed cinnamyl ester form of parental compound

taraxerol, isolated from Bruguiera cylindrica displayed cytotoxic activity against mouse

neuroblastoma Neuro 2A cell line [40]. Moreover, most of the study has been focused on the

anticancer activity but their mode of action and molecular interaction are unknown. In the

future, it will very important to explore the mechanism of bioactive compounds. Till date, the

number of anticancer bioactive compounds isolated from mangrove species which are

comparable to the activity of a commercially available anticancer drug. Hence, there is an

alternative way to increase the efficacy of available anticancer compounds through chemical

synthesis. Apart from this very few reports are available on pharmacokinetic studies of

mangrove origin bioactive compounds. A thorough investigation of mangrove species may be

a source of novel anticancer agents with structurally diverse compounds and this could pave

the way for a potential anticancer drug. The chemical structures of the anticancer bioactive

compound were given in the Figure 1 and it can be active ingredients for formulation of novel

broad-spectrum anticancer agents.

2.2 Antimicrobial activities of isolated compounds

In recent years, resistance among the pathogenic organisms towards the synthetic

antimicrobials has been increased and it has become a leading cause of death worldwide [41].

Moreover, due to side effects of existing chemotherapeutic agent and the resistance

developed, plant derived compounds have been received more attention as a potential source

of the future drug. A new isopimarane, Isopimar-8(14)-en-16-hydroxy-15-one (39) obtained

from the roots of C. tagal, were screened for antibacterial activity. It exhibits antibacterial

activity against Streptococcus pyrogens, Salmonella pooni, Bacillus cereus, Staphylococcus

aureus and Micrococcus kristinae [42]. Moreover, antifouling activity against Pseudomonas

pseudoalcaligenes of atisane-type diterpene, ent-16α-hydroxy-atisane-3,4-lactone (40) from

E. agallocha was reported [43]. Four new isomeric macrolides of combretastatin D-2

congeners named isocorniculatolide A (41), 11-O-methylisocorniculatolide A (42), 11-

Omethylcorniculatolide A (43) and 12-hydroxy-11-O-methylcorniculatolide A (44), were

isolated from A. corniculatum. It was proposed that the antimicrobial activity of an isolated

compound is possibly due to the synergy between metabolites, or alternatively, the most

active metabolites were not yet isolated [44]. A. corniculatum extract demonstrated

effectiveness against Mycobacterium tuberculosis as well [45]. The efficacy of these extracts

against tuberculosis required further investigation of Aegiceras species as antituberculosis

agents. The Acornine 1 (45) and 2 (46) compounds, have antifungal activities and isolated

from the bark of A. corniculatum. Partial structural characterization of these two compounds
indicated that they are oleanane triterpenoids with linked sugar moieties. While both the

compounds exhibited growth inhibition of the Gram-positive bacteria Bacillus subtilis and

Bacillus coagulans while acornine 2 in particular demonstrated strong antifungal activities

against Candida albicans, Trichophyton mentagrophytes and Trichophyton rubrum [46].

Similarly, a new antifungal lactone was isolated from the leaves of X. granatum. Its structure

was elucidated as 3-(1-hydroxyethyl)-4,4-dimethyl-4-butyrolactone (47) and showed a 67.4%

inhibition rate against wheat powdery mildew [47]. Even more, compounds in the natural

products such as the polyphenols and limonoids have been investigated for their antiviral

effects [48]. Four new polyphenols namely excoecariphenols A-D (48-51) were isolated from

the E. agallocha but excoecariphenols A-B showed the unusual flavanebased 1-

thioglycosides. The isolated polyphenols excoecariphenol D showed potential inhibition

against HCV NS3-4A protease enzyme and inhibited HCV RNA in huh 7.5 cells [49]. A new

mexicanolidelimonoids, named sundarbanxylogranins B (52), were isolated from the seeds of

X. granatum found to exhibit moderate anti-HIV activity [50] (Figure 2). Besides, the

inhibitory effect of mangroves derived bioactive compounds requires more investigation to

make it potential antimicrobial agent against bacterial, fungal and viral infections. There are

very few mangrove species investigated for antimicrobial compound and need to be explored

more.

2.3 Anti-inflammatory and antioxidant activities of isolated novel compounds

The secondary metabolites obtained from plants have promising anti-inflammatory activity.

The mechanism of action of anti-inflammatory activity involves reduction in the formation of

inflammation causing factors like nitric oxide through the stimulation of macrophages by

plant secondary metabolites like lipopolysaccharides. Limonoids named thaixylomolins A-C

(53-55), with two new motifs isolated from the seeds of a Thai mangrove, X. moluccensis.
Thaixylomolin B exhibited inhibitory activity against nitric oxide production in

lipopolysaccharide and IFN-γ-induced RAW264.7 murine macrophages [51]. Phenolics are a

heterogenous compound derived from plant secondary metabolism. Phenolic compounds can

be classified into flavonoid and non-flavonoid [52]. Several phenolic and flavonoids

compounds showed anti-inflammation as well as antioxidant properties [53-54]. Although the

anti-inflammation mechanism is not properly known, however it has been stated that

supplementing antioxidant can lower IL-6 level in blood [55]. Epidemiologic data showed

that high phenol diets reduced the occurrence of chronic diseases such as diabetes,

cardiovascular disease, alzheimer, parkinson, and inflammation [56]. A new flavanol

derivative dihydrocaffeic acid-(3→8)-epicatechin (56) were isolated from the stem bark of a

mangrove plant X. granatum and showed an ability to scavenge DPPH radical [57]. A new

andirobin, thaimoluccensin A (57) and new phragmalin-type limonoids, thaimoluccensins B

(58) and C (59) along with a known compound 7-deacetylgedunin (60) were isolated from

seeds of a Thai mangrove plant, X. moluccensis. Among the isolated new compound only 7-

deacetylgedunin exhibited significant inhibitory activity against nitric oxide production from

activated macrophages suggesting that the compound has anti-inflammatory activity [58].

Chemical examination of the stems and twigs of E. agallocha resulted in the isolation of six

ent-kauranediterpenoids named agallochaols K-P (61-66) and an atisane-type diterpenoid

agallochaol Q (67). Only the agallochaols K, O, P and Q suppress the expression of Nuclear

Factor kappa-B (NF-κB) and activator protein (AP-1) targeted genes including TNF-α and

IL-6. In addition, agallochaols K, O, P and Q block NF-κB activation, while agallochaols K

and Q block AP-1 activation indicates that, the ability of these compounds to acts as in vitro

anti-inflammatory agent [59]. Further, chemical investigation of K. candel resulted in the

isolation of new sesquiterpene glycoside, kandelside (68) and three megastigman glycoside

compounds (69-71). Isolated compounds were also evaluated for their inhibitory effects on
the production of pro-inflammatory cytokines interleukin (IL)-12 p40, IL-6, and tumor

necrosis factor a (TNF-a) in lipopolysaccharide (LPS)-stimulated bone marrow-derived

dendritic cells. Among these compounds, compound (71) exhibited strong inhibitory activity

against IL-6 production and TNF-a production but exhibited no activity on IL-12 p40

production [60]. The fruit of the mangrove Avicennia marina used for the chemical

investigation showed the presence of a new caffeic acid derivative, maricaffeolylide A (72),

and a new megastigmane derivative, maricyclohexene A (73). The antioxidant ability of these

two compounds was evaluated by a new approach, a cellular antioxidant assay [61].

Similarly, the antioxidant activity of a new 8-hydroxyquercetagetin glycoside (74), namely

brugymnoside A isolated from B. gymnorhiza was also reported [62]. Moreover, two

oleanenes (75-76), belongs to class of rare natural pentacyclic triterpenoids, namely, olean-

18(19)-en-3b-yl-(3,6-dimethyl-3E,6Z-dienoate) and (13a)-27-frido-olean-14(15)- en-(17a)-

furanyl-3b-ol were obtained from R. mucronata. The furanyl oleanene exhibited significantly

greater antioxidative activities than prenylated oleanene [63] (Figure 3).

2.4 Other miscellaneous activities of isolated novel compounds

There has been considerable interest in the phytochemistry and medicinal properties of

mangroves and associated species [25], and the uses of mangrove species in pest control and

as insecticides. The crude extracts of different parts (leaf, bark, root, stilt root, hypocotyls,

and flower) of Rhizophoraceae mangrove species such as, B. cylindrica, C. decandra, R.

mucronata and R. apiculata were studied for insecticidal activity against the dengue vector

Aedes aegypti. It was proposed that stilt root extract of R. mucronata is the potential source of

novel insecticidal compounds [64]. Six new phragmalins, moluccensins H-M (77-82), two

new andirobin-type limonoids moluccensins N-O (83-84) and two new tirucallane derivatives

moluccensins P-Q (85-86) were isolated from X. moluccensis. The moluccensins H-I exhibit
antifeedant activity towards third-instar larvae of Brontispa longissima. Further, limonoids

with similar activity such as godavarin A (87), godavarin D (88) [65] and Moluccensin R (89)

[66] were reported. Plant secondary metabolites are effective against the infection of

Helicobacter pylori and it also inhibits the in-vitro anti-ulcer activity. Gastric ulcer is a very

common gastrointestinal disorder affecting a large number of people worldwide. The

antiulcerogenic activity of xyloccensins X+Y (90), isolated from X. moluccensis was

reported. It has been proposed that antiulcerogenic activity might be due to its antisecretory

activity [67]. Other activities such as the antidiabetic properties [68], neuropharmacological

effects [69] and new dimeric alkylbutenolide, paracaseolide A (91) have been reported from

S. paracaseolaris [70] exhibits significant inhibitory activity against enzyme phosphatase

CDC25B (Figure 4).

3. Novel compounds

Mangroves species are rich in bioactive compounds and can serve as a reservoir for new

bioactive compounds such as amides, alkaloids, flavonoids, tannins, saponins, glycosides,

terpenoids, and phenolic compounds. They are widely reported to be present in the seeds,

leaves, and stem bark of mangrove species [71]. The pharmacological activities of phenolics,

terpenoids, and limonoids from mangrove species indicate that they can serve as health

promoting and pharmaceutical agents. These groups of compounds, which often contain

aromatic rings with hydroxyl or sulfur groups, naturally occur in most plants [72].

Diterpenes are the most abundantly isolated secondary metabolite from E. agallocha [71].

New class secolabdanoid, derived from a labdane skeleton (excolides A-B) with an

unprecedented framework was isolated from the stem of E. agallocha along with a revision

of rhizophorin A structure [73]. Additionally, ent-isopimarane diterpenes, agallochaexcoerins

D-F were isolated successfully from E. agallocha, while F consists of unusual seven-
membered lactone moiety. [74]. X. granatum mangrove is medicinally important and several

types of chemically diverse compounds reported from it [75-76]. In last decade, several new

compounds were reported from Xylocarpus species like alkaloid namely granatoine and

xylocarpin L [77], Limonoids such as, thaixylomolins D-F, granatumins V-Y,

Andhraxylocarpins A-E, granatumins H-I, hainangranatumins A-J, Godavarin K, [78-84],

tetranortriterpenoids [85-86]. Despite, this new diterpene, tagalenes G-I, tagalsin L-N [87-88]

and lupane type triterpene [89] were reported from C. tagal.

4. Conclusion and future perspectives

This review summarizes representative substances derived in the last decade from mangrove

plants. It indicates that mangroves are an inexhaustible source of new molecules that often

display unique structures and sometimes have very interesting pharmacological properties,

such as anticancer, antibacterial, antifungal, antiviral, anti-inflammatory, antioxidant and

other activities. However, according to literature information, only a few species of

mangroves have been extensively investigated for the evaluation of their chemical profile.

Among isolated constituents, terpenoids and limonoids are the most representative

compounds. Several new limonoids have been identified in X. granatum and X. moluccencis.

These compounds might be considered as chemotaxonomic markers of the genus. Therefore,

in order to confirm the possibilities to use these metabolites as taxonomic markers detail

investigation has to be done on Xylocarpus species. The activities shown by these compounds

can be attributed for development of a drug.

Despite the fact, phytochemical and biological studies on mangrove species have received

considerable interest, Most of the studies are aimed at evaluating the bioactive potential of

crude extracts and it is necessary to characterize biological activity of isolated novel

compounds by using in vivo models rather than in vitro approach. Moreover, detailed studies
are required to investigate mangrove species that have never been chemically and

biologically studied. However, the purpose of this review is to establish the foundation for

further studies on mangroves plant.

Consent for publication

Not applicable.

Conflict of interest

The authors declare that they have no conflict of interest.

Acknowledgements

The work in KK lab was supported by a grant from Council of Scientific and Industrial

Research, India (38(1416)/16/EMR-II). NLS is gratefully acknowledged to Council of

Scientific and Industrial Research, India for providing Junior Research Fellowship. AAS is

gratefully acknowledged to BITS Pilani, K K Birla Goa campus, Goa, India for the research

fellowship.

Authors’ contributions

All authors were involved in writing and reviewing the manuscript.

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