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MINI-REVIEW
Received: 27 August 2014 / Revised: 14 December 2014 / Accepted: 15 December 2014 / Published online: 31 December 2014
# Springer-Verlag Berlin Heidelberg 2014
Abstract In recent decade, seaweeds-associated microbial communities have been significantly evaluated for functional and
chemical analyses. Such analyses let to conclude that
seaweeds-associated microbial communities are highly diverse
and rich sources of bioactive compounds of exceptional molecular structure. Extracting bioactive compounds from seaweedassociated microbial communities have been recently increased
due to their broad-spectrum antimicrobial activities including
antibacterial, antifungal, antiviral, anti-settlement, antiprotozoan,
antiparasitic, and antitumor. These allelochemicals not only provide protection to host from other surrounding pelagic microorganisms, but also ensure their association with the host.
Antimicrobial compounds from marine sources are promising
and priority targets of biotechnological and pharmaceutical applications. This review describes the bioactive metabolites reported from seaweed-associated bacterial and fungal communities
and illustrates their bioactivities. Biotechnological application
of metagenomic approach for identifying novel bioactive metabolites is also dealt, in view of their future development as a strong
R. P. Singh (*) : P. Kumari : C. R. K. Reddy (*)
Discipline of Marine Biotechnology and Ecology, CSIRCentral
Salt and Marine Chemicals Research Institute,
Bhavnagar 364002, Gujarat, India
e-mail: ravindrapal.1441@gmail.com
e-mail: crk@csmcri.org
R. P. Singh
Laboratory of Microbial Technology, Department of Bioscience and
Biotechnology, Faculty of Agriculture, Kyushu University,
Fukuoka 812-8581, Japan
P. Kumari
Institute of Plant Sciences, Agricultural Research Organization
(ARO), Volcani Center, PO Box 6, Bet Dagan 50250, Israel
C. R. K. Reddy
Academy of Scientific and Innovative Research (AcSIR),
New Delhi, India
Introduction
Marine waters comprise a high diversity of microbial life, predominantly including bacteria, fungi, viruses, spores, and actinomycetes (Engel et al. 2002; Harder 2009). These organisms also
settle on marine animals and plants, besides occurring in sea
surface, and form unique associations with their hosts (Lafi
et al. 2005; Webster et al. 2008; Singh and Reddy 2014).
Associated microorganisms utilize nutrients (e.g., carbon) source
produced by their host and in return protect them from harmful
entities in surrounding by secretion of certain biological active
molecules called bioactives (Armstrong et al. 2001; Jiang et al.
2001; Jamal et al. 2006; Lane and Kubanek 2008). Seaweeds are
part of highly productive ecosystems and are habitats of numerous bioactive compounds producing microorganisms. Bioactive
compounds obtained from associated microorganisms are known
for broad range of biological effects such as antimicrobial,
antisettlement, antiprotozoan, antiparasitic, and antitumors
(Egan et al. 2001, 2008; Penesyan et al. 2011; Lee et al. 2013).
For example, Egan et al. (2001; 2002) identified a number of
Pseudoalteromonas strains from surface of Ulva australis that
exhibited antisettlement activity against invertebrate larvae and
algal spores as well as antibacterial and antifungal activities.
Mostly, bioactive compounds producing microorganisms are
evolved through high competitive environment due to nutrient
and space limitation on their host surface that led them to produce
Fig. 1 Graphical represent of green seaweed, existing of bacterial and fungal communities on their surface and structure of bioactive compounds
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Vibrio costicolus has a unique Na+ -dependent NADHquinone reductase that functions as a primary Na+ pump and
is required for its maximum activity (Unemoto et al. 1977;
Hayashi et al. 2002). The Na+-translocating NADH-quinone
reductase (NQR) of V. alginolyticus is composed of six structural genes, namely nqrA, nqrB, nqrC, nqrD, nqrE, and nqrF
(Beattie et al. 1994; Hayashi et al. 1994; 1995). It has been
found that korormicin specifically inhibited the NQR complex
of these marine halophilic Vibrio species (Nakayama et al.
1999). Later, homology search of the nqr operon revealed that
the Na+-pumping NQR complex is widely distributed among
gram-negative pathogenic bacteria (Hayashi et al. 2002). This
drug is potentially suggested for pharmaceutical application.
Recently, Tebben et al. (2014) identified 13 natural products from Pseudoalteromonas strain J010, which were isolated from surface of the crustose coralline alga Neogoniolithon
fosliei. Among them, a new bromopyrrole, 4-((3,4,5-tribromo1H-pyrrol-2-yl) methyl)phenol and five new korormicins G
K were obtained which exhibited antibacterial activity.
Interestingly, this strain also produced a coral larval metamorphosis inducer compound, tetrabromopyrrole which had a
broad-spectrum activity against the tested bacteria, fungi,
and protozoan (Tebben et al. 2011, 2014).
Two more novel compounds (violacein and YP1) were
obtained from U. australis associated with P. tunicata
(Franks et al. 2006; Matz et al. 2008). Violacein (an alkaloid)
producing P. tunicata and P. ulvae showed antiprotozoal activity against amoeba Acanthamoeba castellanii at nanomolar
concentration (Matz et al. 2008). It also demonstrated that
violacein induces apoptosis-like cell death program in protozoan predators. It has been observed that violacein produced
by Chromobacterium violaceum induces apoptosis in mammalian cell lines (Ferreira et al. 2004; Kodach et al. 2006).
Therefore, it could be a novel therapeutic agent to treat cancerous cells (Matz et al. 2008). Recently, Subramaniam et al.
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Seaweed host
Seaweed-associated fungi
Acrosiphonia arcta
Geomyces sp., Metschnikowia australis, Penicillium sp., Candida sake, Cladosporium sp., Godinho et al. 2013
Cladosporium tenuissimum, Debaryomyces hansenii, Mortierella sp., Phoma sp.,
Thelebolus globosus
Aspergillus spp., Aureobasidium pullulans, Chaetomium spp., Cladosporium spp., Fusarium Suryanarayanan et al. 2010
spp., Mucor sp., Penicillium spp., Phoma sp., Pyrenochaeta sp.
Aspergillus spp., Chaetomium spp., Curvularia spp., Paecilomyces spp., Penicillium spp.
Suryanarayanan et al. 2010
Caulerpa racemosa
Caulerpa
scalpelliformis
Caulerpa
Aspergillus spp., Chaetomium spp., Cladosporium spp., Fusarium spp., Myrothecium sp.,
sertularioides
Penicillium spp., Phialophora sp.
1
1
Desmarestia
[Metschnikowia australis, Penicillium sp.], 2[Geomyces pannorum
menziesii,
2
D. anceps
Halimeda macroloba Aspergillus spp., Chaetomium spp., Paecilomyces spp., Penicillium spp., Trichoderma sp.
Monostroma hariotii
Ulva lactuca
Ulva fasciata
Ulva intestinalis
References
Gelidiella acerosa
Gracilaria spp.
Grateloupia
lithophila
Halymenia spp.
Aspergillus sp., Cladosporium spp., Drechslera spp., Emericella nidulans, Paecilomyces spp.,
Penicillium spp., Phoma sp.
Palmaria decipiens 1[Penicillium sp., Geomyces sp., Acremonium sp., Fusarium sp., Yamadazyma mexicana,
Aspergillus sp., Chaetomium sp., Penicillium spinulosum] 2[Cryptococcus carnescens]
Seaweed host
Seaweed associated Fungi
Portieria hornemanii Aspergillus sp., Cladosporium spp., Memnoniella sp., Penicillium spp., Phomopsis sp.,
Trimmatostroma sp.
Pyropia endiviifolia Cladophora maronum, Penicillium spp., Pseudogymnoascus spp., T. globosus, Aspergillus
sp., Aspergillus protuberus, Antarctomyces psychrotrophicus, Cladosporium lignicola,
Mortierella antarctica, Oidiodendron truncatum, Metschnikowia australis, Dipodascus
australiensis, Meyerozyma guilliermondii, Verticillum sp., Lecanicillium sp.
1
Adenocystis spp.
[Penicillium spp., Aspergillus conicus, Geomyces sp., Debaryomyces hansenii, Meyerozyma
caribbica] 2[Antarctomyces psychrotrophicus, Geomyces pannorum, Oidiodendron sp.,
Penicillium sp., Phaeosphaeria herpotrichoides, Algicolous fungi]
Ascophyllum
Aspergillus fumigatus, Lichtheimia corymbifera, Cladosporium sp., Dendryphiella salina
nodosum
Dictyota dichotoma Aspergillus spp., Trichoderma sp.
Fucus vesiculosus
[Lindra, Lulworthia, Engyodontium, Sigmoidea/ Corollospora complex, and Emericellopsis/ Zuccaro et al. 2008, 2Flewelling
Acremonium-like ribotypes], 2[Aspergillus fumigatus, Coniothyrium sp., Penicillium sp.,
et al. 2013
Coniothyrium sp.]
Aspergillus fumigatus, Coniothyrium sp., Penicillium sp., Alternaria sp.
Flewelling et al. 2013
Fucus spiralis
Penicillium sp.
Fucus serratus
Lobophora variegata Aspergillus spp., Chaetomium spp., Emericella nidulans, Nigrospora sp.
Padina
tetrastomatica
Acremoniella sp., Aspergillus spp., Chaetomium spp., Monodictys sp., Paecilomyces spp.,
Penicillium spp.
Table 1 (continued)
Seaweed host
Seaweed-associated fungi
References
Padina gymnospora
Aspergillus spp., Chaetomium spp., Cladosporium spp., Phoma sp., Trichoderma sp.
Phaeurus antarcticus Penicillium sp., Geomyces sp., Aspergillusterreus, Eurotium herbariorum, Eurotium repens, Godinho et al. 2013
Penicillium steckii
Plocamium
Metschnikowia sp., Acremonium sp., Cladosporium sp., Penicillium biourgeianum
Flewelling et al. 2013
cartilagineum
1
Sargassum sp.
[Corollospora sp.], 2[Alternaria spp., Aspergillus spp., Colletotrichum sp., Drechslera spp., 1Schulz et al. 2008,
2
Suryanarayanan et al. 2010
Helicosporium sp., Nigrospora sp., Taeniolella sp., Varicosporium sp.]
Sargassum wightii
Stocheospermum
marginatum
Turbinaria spp.
Aspergillus spp., Cladosporium spp., Emericella nidulans, Nigrospora sp., Oidiodendron sp., Suryanarayanan et al. 2010
Paecilomyces spp.
Alternaria spp., Aspergillus spp., Chaetomium spp., Emericella nidulans, Nigrospora sp.
Suryanarayanan et al. 2010
Aspergillus spp., Chaetomium spp., Cladosporium spp., Colletotrichum sp., Curvularia spp., Suryanarayanan et al. 2010
Drechslera spp., Emericella nidulans, Fusarium spp., Monodictys sp., Nigrospora sp.,
Paecilomyces spp., Phaeotrichoconis sp., Phialophora sp., Phoma sp.
Additionally, it has been found that endophytes produce antioxidant chemicals that protect their host plants from diseases,
drought, and heavy metal toxicity by increasing tolerance of
the host to oxidative stress (White and Torres 2010).
Flewelling et al. (2013) demonstrated that the mycelial and
broth extracts from endophytic fungal isolates isolated from
different seaweeds showed potent bioactivities wherein, 15
extracts had antimicrobial activities with >80 % inhibition
against S. aureus, P. aeruginosa, and Candida albicans.
Also, seven extracts obtained from Microdochium sp. (isolated from Porphyra sp.), Sterile Pigmented II and III (isolated
from Ulva intestinalis), Penicillium sp. V and VI (isolated
from Fucus spiralis) had larvicidal activities with a LC50 <
100 g/mL. Mathan et al. (2013) screened 19 seaweed endophytic fungal strains for their bioactivity against human and
fish pathogenic bacteria such as E. coli, S. aureus,
V. parahaemolyticus, Klebsiella oxycota, V. cholera, and fish
bacterial pathogens, Aeromonas hydrophila, Enterobacter
aerogens, Flavobacterium sp., Micrococcus sp., and
P. fluorescens of which six strains showed >10 mm of zone
of inhibition. These authors proposed that antibacterial
activity might be due to the presence of bioactive
metabolites produced by the seaweed endophytic fungi.
Recently, Furbino et al. (2014) collected 239 fungal isolates
from 390 thalli of the endemic Antarctic macroalgae,
Monostroma hariotii and Pyropia endiviifolia, and found that
extracts of these endemic and cold-adapted fungi displayed
biological activities. Only six fungal taxa potentially showed
antifungal activity with 6196 % of inhibition. The extracts of
Pseudogymnoascus sp., Guehomyces pullulans, and
Metschnikowia australis showed selective antifungal activities against C. albicans, Candida krusei, and Cladosporium
sphaerospermum. The extract of Dipodascus australiensis
inhibited selectively the growth of C. albicans; G. pullulans,
M. australis, and Pseudogymanoascus sp. 1 were selective
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compound with a rare tetrahydro-2H-benzofuro[7-b][1,4]dioxin9(3H)-one skeleton (Fig. 3d) and showed cytotoxicity against A549 (IC50 80.7 mol/L) and HL-60 cell lines (IC50 143.1 mol/
L). Gamal-Eldeen et al. (2009) isolated a new chromone derivative, chromanone A [2-(hydroxymethyl)-8-methoxy-3-methyl4H-chromen-4-one] (Fig. 3e) from Penicillium sp. associated
with Ulva sp., that exhibits anti-tumorigenesis properties via
modulation of carcinogen metabolizing enzymes (such as
NADPH-cytochrome P-450 (NADPH-CYP) reductase or isozymes of CYP or glutathione S-transferases) and protection from
DNA damage.
Gao et al. (2011a) extracted several tetracyclic diterpenes,
conidiogenones from Penicillium chrysogenum QEN-24S associated with red alga Laurencia sp., of which conidiogenone B
showed potent activity against methicillin resistant S. aureus,
Staphylococcus epidermidis, P. aeruginosa, and P. fluorescens
(each with a MIC value of 8 g/mL) along with a week antifungal activity against C. albicans (MIC, 128 mg/mL) whereas
conidiogenol showed activity against P. fluorescens and
S. epidermidis (each with a MIC value of 16 g/mL). In another
study of chemical investigation of this fungus (P. chrysogenum
QEN-24S) led to discoveries of four new compounds, polyketide derivative penicitides A and B, 2-(2,4-dihydroxy-6methylbenzoyl)-glycerol, and penicimonoterpene. Among
them, penicitides A displayed cytotoxic activity against the
human hepatocellular liver carcinoma, HepG2 cell line (IC50
32 g/mL) while penicimonoterpene showed strong inhibitory
activity against plant pathogenic insect Alternaria brassicae in
dual culture test with 17 mm inhibition zone at the concentration of 20 g/disk (Gao et al. 2011b). Further, extensive spectroscopic analysis revealed two more novel polyoxygenated
steroids compounds, namely, penicisteroids A and B (Gao
et al. 2011c). Penicisteroids A is structurally unique compound
containing tetrahydroxy and C-16-acetoxy groups and showed
potent antifungal activity against A. niger with a clear inhibition
zone of 18 mm diameter at the concentration of 20 g/disk. It
also displayed selective activity against the tumor cell lines
HeLa, SW1990, and NCI-H460 with the IC50 of 15, 31, and
40 g/mL respectively.
Two pinophilins, a class of hydrogenated azaphilones along
with the co-isolated metabolite Sch 725680 were isolated from
Penicillium pinophilum associated with Ulva fasciata. These
compounds selectively inhibited the activities of mammalian
DNA polymerases (pols), A (pol g), B (pols a, d, and 3), and
Y (pols h, i, and k) families and the growth and proliferation of
several human tumor cell lines (Myobatake et al. 2012).
ascosalipyrrolidinone A (3R,4S,5S,6S,8R,10R)-3-[1,2,4a,5,6,
7,8,8a-octahydro-3,6,8-trimethyl-2-[(E)-1-methyl-1propenyl]-1-naphthalenyl]carbonyl-5-butoxy-1,5-dihydro-5methyl- 2H-pyrrol-2-one) from endophytic obligate marine
fungus Ascochyta salicorniae associated with Ulva sp. This
compound displayed antiplasmodial activity toward
Plasmodium falciparum strains K1 (IC50 736 ng/mL) and
NF 54 (IC50 378 ng/mL). It also showed antimicrobial activity
against Bacillus megaterium (5 mm), Mycotypha
microsporum (4 mm), and Microbotryum violaceum (2 mm)
at a concentration of 50g per filter disk and inhibited tyrosine
kinase p56lck to 70 % of its activity at a concentration of
40g/mL and to 23 % at a concentration of 200g/mL.
Wang et al. (2006) identified A novel 2H-benzopyran derivative, chaetopyranin exhibiting moderate DPPH radical scavenging activity (IC50 35 g/mL) and a weak to moderate cytotoxic activities against three tumor cell lines human microvascular endothelial cells, HMEC (IC50 15.4 g/mL), hepatocellular carcinoma cells, SMMC 7221 (IC50 28.5 g/mL), and
human lung epithelial cells, A549 (IC50 39.1 g/mL). This
compound was isolated from Chaetomium globosum derived
from Polysiphonia urceolata (Wang et al. 2006).
Naganuma et al. (2008) reported 1-deoxyrubralactone, a
novel specific inhibitor of families X (rat pol ) and Y (human
pol ) of eukaryotic DNA polymerases from a fungal strain
derived from sea algae. Its IC50 values on family X and
family Y were 11.9 and 59.8 M, respectively. Pontius et al.
(2008b) isolated a novel heterodimeric chromanone compound,
noduliprevenone exhibiting cancer chemopreventive potential
from algal endophytic fungus Nodulisporium sp. This compound contained two uniquely modified xanthone-derived
units, including four chiral centers and a chiral axis. This compound was found to be a competitive inhibitor of cytochrome
(P450) 1A activity with an IC50 value 6.51.6 M and induced
at the same time twofold NAD(P)H:quinone reductase (QR)
activity in Hepa 1c1c7 mouse culture cells with a concentration
of 5.31.1 M. Pontius et al. (2008c) also isolated two dimeric
xanthone derivatives, monodictyochromes A and B from
algicolous fungus Monodictys putredinis. Both these compounds displayed cancer chemopreventive potential and
inhibited cytochrome (P450) 1A activity with IC50 values of
5.3 and 7.5 M, respectively, as well as aromatase inhibitory
activity, with IC50 values of 24.4 and 16.5 M. In addition, they
displayed moderate activity as inducers of QR in cultured
mouse Hepa 1c1c7 cells, with CD values (concentration required to double the specific activity of QR) of 22.1 and
24.8 M, respectively. Moreover, Thirunavukkarasu et al.
(2011) and Suryanarayanan et al. (2012b) showed that fungal
endosymbionts of seaweeds (such as Alternaria, Chaetomium,
Cladosporium, Colletotrichum, Curvularia, Nigrospora,
Paecilomyces, Phaeotrichoconis, Phoma, and Pithomyces are
a good source of the therapeutic enzyme L-asparaginase which
is used in the treatment of acute lymphoblastic leukemia.
1581
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