A Comprehensive Review of Secondary Metabolites with

Antialgal Activity from Marine Macroalgae against Red

Tide Microalgae

Authors: Sun, Yingying, Dong, Shasha, Zhou, Wenjing, Guo, Lei, Guo,
Gan-Lin, et al.
Source: Journal of Coastal Research, 93(sp1) : 475-488
Published By: Coastal Education and Research Foundation
URL: https://doi.org/10.2112/SI93-062.1

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 Journal of Coastal Research SI 93 475–488 Coconut Creek, Florida 2019

A Comprehensive Review of Secondary Metabolites with Antialgal

Activity from Marine Macroalgae against Red Tide Microalgae
Yingying Sun†‡*, Shasha Dong†, Wenjing Zhou†, Lei Guo†, Gan-Lin Guo†§, and Xin Zhang†

Jiangsu Key Laboratory of Marine

†
Co-innovation Center of Jiangsu
‡
Jiangsu Key Laboratory of Marine
§

Bioresources and Eco-environment Marine Bio-industry Technology Biotechnology

Huaihai Institute of Technology Lianyungang 222005, China Huaihai Institute of Technology www.cerf-jcr.org
Lianyungang 222005, China Lianyungang 222005, China

ABSTRACT

Sun, Y.; Dong, S.; Zhou, W.; Guo, L.; Guo, G., and Zhang, X., 2019. A comprehensive review of
secondary metabolites with antialgal activity from marine macroalgae against red tide microalgae. In:
Guido-Aldana, P.A. and Mulahasan, S. (eds.), Advances in Water Resources and Exploration. Journal of
Coastal Research, Special Issue No. 93, pp. 475–488. Coconut Creek (Florida), ISSN 0749-0208.

www.JCRonline.org Red tide, mainly caused by the large-scale reproduction of microscopic algae, has virtually affected every coastal
country or region in the whole world over the last several decades. In order to control and mitigate the proliferation
and diffusion of red tide microalgae, there are many methods or strategies for fighting or inhibiting red tide
microalgae species, these methods or strategies included mechanical, chemical, biological, genetic methods and
others. Unfortunately, the use of these methods or strategies is usually ineffective. There are some evidences that
the inhibition effect of marine macroalgae on the growth of red tide microalgae is mainly due to the release of
bioactive molecules, which are mainly secondary metabolites. Thus, antialgal secondary metabolites, isolated
marine macroalgae, have become an environmentally friendly alternative approach. And relevant researches of
antialgal secondary metabolites in marine macroalgae, such as screen, isolation, identification and other research
etc., have also become very important subjects to biological control of red tide microalgae. The inhibition effects
of marine macroalgae on red tide microalgae are here reviewed, focusing on antialgal secondary metabolites,
isolated from marine macroalgae, against red tide microalgae growth. Further, this paper describes isolation
and EC50-96 h (half maximal effective concentration) or IC50-96 h (half maximal inhibitory concentration) for red
tide microalgae of some antialgal secondary metabolites, including the recently discovered compounds. Finally,
this review is the first to demonstrate that development relationships between macroalgae and red tide using
CiteSpace, and cluster view of macroalgae and red tide is given for the first time. This work provides scientists in
the field with the necessary information and the urgent need to isolate and identify screening antialgal secondary
metabolites in different marine macroalgae. Also, analysis result, which obtained through CiteSpace, has pointed
out that allelopathic interaction between marine macroalgae and red tide microalgae has been developed into a
study area during the last twenty years.

ADDITIONAL INDEX WORDS: Antialgal secondary metabolites, inhibitory activity, marine macroalgae,
microalgae, red tide.

INTRODUCTION methods (actinomycete, bacteria, algae, shell, zooplankton, fishes

Red tide, also called harmful algal blooms (HABs), occur
frequently in marine areas, and it poses a serious threat to water
reservoir, fisheries, aquaculture, public health and tourism in the
last decades (Hallegraeff, 2003; Zhou and Zhu, 2006). Therefore,
the control and mitigate the proliferation and diffusion of HAB
is important and urgently required issue for marine environment
protection. Different strategies have been adopted (Kim, 2006),
such as physical treatment (barriers, filters, pumps, carbon
absorption, ultra-sonic disturbance, and ultraviolet irradiation,
etc.) (Visser et al., 2005), chemical manipulation (clay minerals,
copper sulfate, yellow loess, organic amines, and so on) (Choi et
al., 1998; Holdren, Jones, and Taggart, 2001; Sandrini, Huisman,
and Matthijs, 2015; Seder-Colomina et al., 2013), and biological
DOI: 10.2112/SI93-062.1 received 22 May 2018; accepted in revision
24 March 2019.
*Corresponding author: syy-999@163.com
©
Coastal Education and Research Foundation, Inc. 2019
and others) (Demeke, 2016; Pajdak-Stós, Fiałkowska, and Fyda,
2001).
Marine macroalgae, are considered to be a potential source
of secondary metabolites with wide variety of biology activity,
including antialgal, antibacterial, antifouling, antioxidant
activities, and so on (El Gamal, 2010). Among these various
metabolites, antialgal secondary metabolites have been found in
many kinds of marine macroalgae including green (Alamsjah et
al., 2005; Jeong et al., 2000; Jin, 2005; Tang and Gobler, 2011)
(Table 1), red (Alamsjah et al., 2005; An et al., 2008; Jeong et al.,
2000; Nan et al., 2004; Xu, 2005; Xu, 2008) (Table 2) and brown
macroalgae (Alamsjah et al., 2005; An, 2008; Bazes et al., 2009;
Cho et al., 1999; Jeong et al., 2000; Kim et al., 2006; Nagayama
et al., 2003; Takedai et al., 2003; Zhang, 2009) (Table 3). Some
reports revealed that releasing of antialgal secondary metabolites
be the inhibitory mode of action with marine macroalgae. It is
now widely accepted that marine macroalgae can produce and
release some secondary metabolites with inhibitory activity into

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 476 Sun et al.

the environment (Alamsjah et al., 2005; Jeong et al., 2000).
Hence, they have drawn great attention (Cui, 2014; Hirao et al.,
2012; Pu et al., 2016; Sun et al., 2016; Sun et al., 2017; Tang et
al., 2015; Ye and Zhang, 2013).
Recently, the isolation of secondary metabolites from marine
macroalgae has been regarded as an environment friendly
alternative to control red tide microalgae in marine systems
(Accoroni et al., 2015; Alamsjah et al., 2005; An et al., 2008;
Ben et al., 2017; Jeong et al., 2000; Nan, Zhang, and Zhao,
2004; Sun et al., 2015; Tang and Gobler, 2011). These secondary
metabolites include a series of biologically active molecules,
for example, monoterpenes (Konig, Wright, and Linden, 1999),
bromide (Ohsawa et al., 2001), polyphenol (Gross, 2003),
phenylpropanoids (Sun et al., 2018a), miscellaneous compounds
(Macίas et al., 2008; Sun et al., 2016; Sun et al., 2017; Sun et al.,
2018a, c), and other not yet identified compounds (Accoroni et al.,
2015; An et al., 2008; Ben et al., 2017; Chowdhury et al., 2014;
Sun et al., 2016; Tang and Gobler, 2011; Wang et al., 2007b).
However, isolation and identification of antialgal secondary
metabolites from marine macroalgae are difficult since there are
no textbook guidelines for extraction and purification. Therefore,
this paper have assembled all available reference materials on
antialgal secondary metabolites in marine macroalgae, including
growth inhibition of marine macroalgae against marine microalgae
(Table 1, Table 2, Table 3), isolation, name of some antialgal
secondary metabolites (Figure 1, Figure 2, Table 4), and EC50-96
h
(half maximal effective concentration) or IC50-96 h (half maximal
inhibitory concentration) of some antialgal secondary metabolites
for red tide microalgae (Tables 5-6).
This study is restricted to a summary of antialgal secondary
metabolites from marine macroalgae, while non-secondary
metabolites with antialgal activity (for example, fatty acids and
their derivatives) are not included here, and their review was
presented by others researchers (Alamsjah et al., 2005; Jin, 2005;
Oh et al., 2010; Suzuki et al., 2001).
In addition, this review is the first to demonstrate that
development relationships between macroalgae and red tide by
using CiteSpace (Chen, 2009), and cluster view of macroalgae
and red tide is given for the first time. This is very important to
promote the development of this field and biological control of
red tide microalgae using macroalgae (mainly using antialgal
secondary metabolites isolated from macroalgae).
METHODS
Utilizing data information from the Web of Science, Springer,
Google Scholar and CNKI, the reliable material sources of this
systematic manuscript paper were obtained from the literatures
published during recent twenty years. Further, to give a more
explicit knowledge, development relationships between
macroalgae and red tide in the last 20 years have been analyzed
by using CiteSpace (Chen, 2009).
RESULTS
Inhibition Effects of Macroalgae on Marine Microalgae and
Antialgal Secondary Metabolites
Tables 1, 2 and 3 summarize the inhibition effects of the
antialgal components from marine macroalgae in Chlorophyta,
Rhodophyta and Ochrophyta against marine microalgae (mainly

Table 1. Inhibition effects of Chlorophyta on marine microalgae.

Chlorophyta Microalgae Antialgal Components References

Caulerpa sp., C. crassa, F. japonica, G. mikimotoi, Methanol or ethanol extract of dry

Alamsjah et al., 2005; Sun et al., 2016
Cladophora sp. H. akashiwo powder
C. polykrikoides, F. japonica, G.
mikimotoi, Methanol or ethanol and water extract Alamsjah et al., 2005; Jeong et al., 2000;
C. fragile H. akashiwo, of dry powder Sun et al., 2016
O. luteus
K. mikimitoi Tannin, organic acids and flavones? Pu et al., 2016
Chladophora sp. H. akashiwo In co-culture conditions Xu, Dong, and Jin, 2005
K. mikimotoi, Fresh tissue, dry powder and aqueous
C. ocellatus Li, Cai, and Liu, 2007
P. minimum extracts of fresh tissue
E. clathrata P. tricornutum Aqueous extracts of fresh tissue Wang et al., 2007a
An et al., 2008; Bie et al., 2011; Tian,
E. clathrata G. breve, S. costatum Aqueous extracts of dry powder
2009
E. linza C. polykrikoides, Methanol and water extracts of dry
Jeong et al., 2000; Wang et al., 2007a
P. donghaiense powder
Alamsjah et al., 2005; Jin, Dong, and
E. linza, F. japonica, G. mikimotoi, Fresh tissues, dry powder, aqueous
Wang, 2005; Sun et al., 2012; Sun et al.,
E. intestinalis, H. akashiwo, O. luteus, and methanol or ethanol extracts of
2016; Wang et al., 2007a; Wang et al.,
U. conglobota P. micans dry tissues
2012; Xu, Dong, and Yu, 2005
A. tamarense,
A. anophagefferens, C. marina,
C. polykrikoides, H. akashiwo, K.
In co-culture conditions, dry powder,
U. lactuca brevis, Nan et al., 2008; Tang and Gobler, 2011
fresh thalli extracts
K. veneficum, Pseudo-nitzschia
multiseries, P. minimum, S.
costatum

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 A Comprehensive Review of Secondary Metabolites with Antialgal Activity from Marine Macroalgae against Red Tide Microalgae477

U. fenestrata Epiphytic microalgae Extracts of dry tissue Nelson et al., 2002

U. fasciata, Ulva sp., F. japonica, G. mikimotoi,
U. pencilliformis H. akashiwo, O. luteus
A. tamarense,
A. carterae, C. gracile,
C. placoidea,
F. japonica, G. breve,
G. mikimotoi, H. akashiwo,
U. prolifera K. mikimitoi,
N. closterium,
O. luteus, P. donghaiense,
P. subcordiformis,
S. costatum,
T. subcordiformis
P. helgolandica
A. tamarense,
C. polykrikoides,
U. pertusa
Cocconeis sp., F. japonica,
G. mikimotoi, H. akashiwo,
K. mikimitoi, O. luteus,
P. donghaiense, S. costatum
U. obscura Epiphytic microalgae
A. pacificum, C. monotis,
U. rigida
O. ovata, P. lima
Methanol extracts of dry powder
Fresh tissue, dry powder, organic
solvent extracts (methanol, acetone,
ethyl acetate, chloroform, ether)
Extracellular products?
Organic solvents extracts (petroleum
ether, acetate, ethanol, distilled water)
Extracts of dry tissue
In co-culture conditions, fresh tissues,
media and dry powder
Alamsjah et al., 2005; Sun et al., 2016
Alamsjah et al., 2005; Bie et al., 2011;
Jeong et al., 2000; Jin and Dong, 2003;
Nan, Zhang, and Zhao, 2004; Nan,
Zhang, and Dong, 2004; Sun, Liu, and
Wang, 2010; Tian, 2009; Wang et al.,
2013
Alamsjah et al., 2005; Ding et al., 2009;
Jin, Dong, and Wang, 2005; Nan, Zhang,
and Li, 2007; Wang et al., 2007b; Wang,
Zhou, and Tang, 2009; Wang et al.,
2013; Xu, Qian, and Jiao, 2005; Zhang
et al., 2006
Nelson et al., 2002; Timothy et al., 2003
Accoroni et al., 2015; Ben et al., 2017

Table 2. Inhibition effects of Rhodophyta on marine microalgae.

Rhodophyta Microalgae Antialgal Components References

A. flabelliformis,
B. atropurpurea,
C. crassicaulis, D. pulvinatum, G. amansii,
G. japonicum,
G. furcata,
G. chouae, Methanol or ethanol extract Alamsjah et al., 2005; Hirao et
G. lemaneiformis, H. akashiwo of dry powder, or in co- al., 2012; Xu, Qian, and Jiao,
G. ramosissima, culture conditions 2005
G. turuturu,
G. flabelliformis,
H. pannosa,
L. undulata,
P. carnosa, P. elliptica, P. haitanensis
Trichodesmium sp., Methanol extract of dry Alamsjah et al., 2005; Manilal et
A. taxiformis
F. japonica, O. luteus powder al., 2010
C. polykrikoides,
C. pilurifera,
F. japonica, Alamsjah et al., 2005;
G. chorda,
G. mikimotoi, Methanol and water Jeong et al., 2000; Oh et al.,
G. chorda,
H. akashiwo, extracts of dry powder 2010; Wang, Xu, and He, 2007;
G. vermiculophylla, P. telfairiae, P. capillacea,
O. luteus, Wang, Tang, and Sun, 2008;
S. marchantioides
P. donghaiense
Methanol extracts of dry
G. intermedia, G. prolongata C. polykrikoides Jeong et al., 2000
powder
A. sanguidea,
A. carterae,
A. tamarense,
Chai, 2016; Lu et al., 2008; Sun
H. akashiwo, Fresh tissue, culture filtrate,
G. lemaneiformis, et al., 2011; Wang et al., 2007a, b;
K. mikimitoi, and methanol extracts of
G. tenuistipitata Wang, Zhou, and Tang, 2009; Wu,
P. donghaiense, dry powder
2017; Yu, Lu, and Yang, 2010
P. micans,
S. costatum,
S. trochoidea

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 478 Sun et al.

H. akashiwo,
Alamsjah et al., 2005; An et al.,
F. japonica, In co-culture conditions,
G. filicina, 2008; Bie et al., 2011; Sun et al.,
G. breve, ethanol or aqueous extracts
P. tenera 2016; Tian, 2009; Xu, Qian, and
G. mikimotoi, of dry powder
Jiao, 2005
S. costatum
C. salina, Methanol extract of dry
H. musciformis Pramitha and Lipton, 2011
I. galbana powder
A. anophagefferens, C. marina,
C. polykrikoides,
K.brevis, Fresh thalli and aqueous
P. purpurea Tang et al., 2015
K. veneficum, extract of fresh thalli
P. minimum,
Pseudo-nitzschia multiseries
A. carterae,
A. tamarense,
C. polykrikoides, Methanol extracts of dry Alamsjah et al., 2005; Jeong et
P. yezoensis
F. japonica, powder al., 2000; Sun et al., 2010
G. mikimotoi, H. akashiwo,
K. mikimitoi, S. costatum
Fresh tissues, media and
R. pseudopalmata O. cf. ovata Accoroni et al., 2015
dry powder

Table 3. Inhibition effects of Ochrophyta on marine microalgae.

Ochrophyta Microalgae Antialgal Components References

C. bullosa, D. undulata,
Chowdhury et al., 2014;
E. cava, E. binghamiae, P.
Methanol or ethanol extracts of dry powder, or in Hirao et al., 2012; Jeong et
coriaceum, C. polykrikoides, H. akashiwo
co-culture conditions al., 2000; Sun et al., 2016;
S. tenuifolium,
Xu, Qian, and Jiao, 2005
S. latiuscula
C. sinuosa, C. cylindrica, D. F. japonica, G. mikimotoi,
Fresh tissues, media, dry powder and/or methanol Accoroni et al., 2015;
dichotoma, D. linearis, D. H. akashiwo, O. luteus,
extracts of dry powder Alamsjah et al., 2005
prolifera O. cf. ovata
C. antiqua,
E. kurome Phlorotannins extract Nagayama et al., 2003
C. polykrikoides, K. mikimotoi
McLachlan and Craigie,
F. vesiculosus M. lutheri, Porphyridium sp. Phenolic substances
1964
C. polykrikoides, F. japonica, G. Alamsjah et al., 2005;
I. foliacea,
mikimotoi, H. akashiwo, Methanol extract of dry powder Hirao et al., 2012; Jeong et
P. crassa
O. luteus al., 2000
Alamsjah et al., 2005; An et
L. japonica, S. fusiforme, Methanol or ethanol, chloroform and aqueous
G. pacificus, S. costatum al., 2008; Bie et al., 2011;
S. pathen extracts of dry powder
Sun et al., 2016; Wu, 2016
C. antiqua, H. akashiwo,
S. horneri Acetone extract of wet tissues Takedai et al., 2003
S. costatum
Alamsjah et al., 2005; An et
S. micracanthum, S. F. japonica, G. mikimotoi,
al., 2008; Bie et al., 2011;
muticum, S. siliquatrum, S. G. pacificus, H. akashiwo,
Methanol or ethanol extracts of dry powder Sun et al., 2016; Wang et
thunbergii, O. luteus, P. micans,
al., 2007a, b; Wang, Wang,
U. pinnatifida S. costatum
and Tang, 2012; Wu, 2016
S. latiuscula P. tricornutum Aqueous extracts of fresh tissue Zhou et al., 2009
Zonaria sp. G. pacificus Methanol extracts of dry powder Wu, 2016

was red tide microalgae, and also included others marine
microalgae), respectively.
Reported researches showed that marine macroalgae are
potential source of antialgal activity compounds. However, so
far, most studies on the effects of marine macroalgae on red
tide microalgae have been limited to co-cultured ecosystems
and some solvent extracts of many marine macroalgae (Table
1, Table 2 and Table 3), there have been few researches into
isolation of antialgal activity compounds of marine macroalgae
(An et al., 2008; Bie et al., 2011; Hirao et al., 2012; Kim et al.,
2006; Lu, 2011; Sun et al., 2015; Sun et al., 2016; Sun et al.,
2017; Sun et al., 2018a, b, c).

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 A Comprehensive Review of Secondary Metabolites with Antialgal Activity from Marine Macroalgae against Red Tide Microalgae479

Dry powders of marine macroalgae

Extraction with acetone or methanol at 25°C for 36 hor 48 h in the darkness

Filtration, evaporation to dryness in vacuo at 45°C

Methanol extracts

Re-dissolving the residue in distilled water

Removal of pigments
Place at 4°C for 24 h in the darkness
Filtration, concentration in vacuo at 60°C

Supernatant fraction

Adjusting to pH 10 or 11 with NaOH (4 N)

Extraction with ethyl acetate

Ethyl acetate phase Aqueous phase

Evaporation to dryness under reduced pressure

FA
Ethyl acetate phase Lower layer

Evaporation to dryness
Adjusting to pH 3 or2 with HCl (1 N)
FB
Extraction with ethyl acetate

Ethyl acetate phase Residual solution

Evaporation to dryness Dialysis for 24 h

Inorganic ions
FC Evaporation to dryness

FD

Filtering though 0.22 μm micron syringe filter

Silical gel column or Sephadex LH-20 column chromatography

Sephadex LH-20 column or preparative thin-layer chromatography (twice)

Structure identification

(HR-ESI-MS, 1H-NMR, 13C-NMR or UV)

Figure 1. Schematic representation of a simplified protocol for isolation and purification of some antialgal secondary metabolites in marine macroalgae (for
details, see reference (Sun et al., 2015; Sun et al., 2016; Sun et al., 2018a, b)).

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 480 Sun et al.

Dry powders of G. lemaneiformis

Extraction with 95% ethanol

Concentration in vacuo at 45 °C

Crude extracts

Adding distilled water

Extraction with petroleum ether

Evaporation to dryness

Petroleum ether phase Aqueous phase

Evaporation to remove petroleum ether

Extraction with ethyl acetate
Silical gel column chromatography
Evaporation to dryness

Ethyl acetate phase Aqueous phase

Evaporation to remove ethyl acetate

Silical gel column or Extraction with n-butanol

Evaporation to remove n-butanol Evaporation to dryness

Sephadex LH-20 column chromatography

Aqueous phase n-butanol phase

HPLC
Macroporous resin column
Silical gel column chromatography chromatography

Sephadex LH-20 column or

ODS chromatography

HPLC or ODS/HPLC chromatography

Structure identification

(HR-ESI-MS, 1H-NMR, 13C-NMR and UV)

Figure 2. Schematic diagram of isolation and purification of some antialgal secondary metabolites in G. lemaneiformis (for details, see reference (Lu,
2011)).

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 A Comprehensive Review of Secondary Metabolites with Antialgal Activity from Marine Macroalgae against Red Tide Microalgae481

Table 4. Antialgal secondary metabolites in marine macroalgae.

Marine Macroalgae Microalgae Antialgal Secondary Metabolites References

Chlorophyta
E. clathrata S. costatum 9-octadecyne? Diisobutyl phthalate? Bie et al., 2011
A.tamarense, Glycerol monopalmitate, 1-O-octadecanoic acid-3-O-β-D- galactopyranosyl
H. akashiwo, glycerol, 9-hexadecenoic acid, 2, 3-dihydroxypropyl ester, 1-O-palmitoyl-
U. prolifera K. mikimitoi, 3-O-β-D-galactopyranosyl glycerol, 1-O-palmitoyl-2-O-oleoyl-3-O-β-D- Sun et al., 2016
P. donghaiense, galactopyranosyl glycerol, loliolide, lsololiolide, zeaxanthin, cholest-5-en-3-
S. costatum ol, pyrrolopiperazine-2, 5-dione
A. tamarense,
a
U. pertusa H. akashiwo, Alkaloids and phenolic acids? Sun et al., 2015
P. donghaiense
A. carterae 3, 7, 11, 15-tetramethyl-2-hexadecen-1-ol, 8-hexadecenol
(-)-dihydromenisdaurilide, 3, 7, 11, 15-tetramethyl-2-hexadecen-1-ol,
H. akashiwo
8-hexadecenol, 17-hydroxyheptadecanoic acid
Trehalose, twenty-two methyl carbonate, 17-hydroxyheptadecanoic acid,
K. mikimitoi
trans-asarone, 2-amino-3-mercaptopropanoic acid
b
U. pertusa Twenty-two methyl carbonate 3, 7, 11, 15-tetramethyl-2-hexadecen-1-ol, Sun et al., 2018c
P. globosa 8-hexadecenol, 17-hydroxyheptadecanoic acid trans-asarone, 2-amino-3-
mercaptopropanoic acid
Trehalose, (-)-dihydromenisdaurilide, isophytol, 17-hydroxyheptadecanoic
P. donghaiense
acid, trans-asarone
Twenty-two methyl carbonate, 17-hydroxyheptadecanoic acid, trans-asarone,
S. costatum
2-amino-3-mercaptopropanoic acid
Rhodophyta
C. pilulifera Epiphytic microalgae CHBr3 Ohsawa et al., 2001
A. carterae Stigmasterol
Gossonorol, stigmasterol, 15-hydroxymethyl-2, 6, 10, 18, 22, 26,
H. akashiwo,
30-heptamethyl-14-methylene-17-hentriacontene, 4-hydroxyphenethyl
P. globosa
alcohol, margaric acid
a
G. lemaneiformis 15-hydroxymethyl-2, 6, 10, 18, 22, 26, 30-heptamethyl-14-methylene-17- Sun et al., 2017
K. mikimitoi
hentriacontene
P. donghaiense Gossonorol, glycerol monopalmitate
Gossonorol, 15-hydroxymethyl-2, 6, 10, 18, 22, 26, 30-heptamethyl-14-
S. costatum
methylene-17-hentriacontene, 4-hydroxyphenethyl alcohol, margaric acid
1-O-palmitoyl -3-O-β-D- galactopyranosyl glycerol, 1-O-palmitoyl
2-O-palmitoleoyl -3-O-β-D- galactopyranosyl glycerol, 1-O-palmitoyl-
b
G. lemaneiformis S. costatum Lu, 2011
2-O-oleoyl-3-O-β-D-galactopyranosyl glycerol, uridine, 8-hydroxy-4E,
6E-octadien-3-on
c
G. lemaneiformis Sun et al., 2018b
H. akashiwo Gossonorol, 7, 10-epoxy-ar-bisabol-11-ol, cyclonerodiol
K. mikimitoi Gossonorol, 7, 10-epoxy-ar-bisabol-11-ol
P. yezoensis Sun et al., 2018a
P. donghaiense Gossonorol, cyclonerodiol
P. globosa, S. costatum Gossonorol
Ochrophyta
H. akashiwo,
D. dichotoma Dictyolactone, sanadaol, dictyol J Kim et al., 2006
K. mikimotoi
A. catenella,
α-monoglyceride, 1-O-palmitoyl-3-O-(6-sulfo--D-quinovopyranosyl)-sn-
I. sinicola H. akashiwo, Hirao et al., 2012
glycerol
K. mikimotoi
Di (2-ethylhexyl) phthalate?
L. japonica S. costatum Diisobutyl phthalate? An et al., 2008
Cyanoacetylurea?
Note: a. collected from the coast of Rizhao, Shandong Province, China; b. collected from aquaculture zone in Nanao Island, Shantou City, Guangdong Province, China; c.
collected from the coast of Rizhao, Shandong Province, China; d. collected from aquaculture zone in Nanao island, Shantou City, Guangdong Province, China.

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 482
Table 5. EC50-96 h (µg/mL) of antialgal secondary metabolites isolated from marine green macroalgae for red tide microalgae.
Red Tide Microalgae
A.carterae
H. akashiwo
K. mikimitoi
a
U. pertusa
P. donghaiense
P. globosa
S. costatum
b
U. pertusa Gymnodinium breve
Note: a. see reference (Sun et al., 2018c); b. see reference (Kang, 2006).
Therefore, further, several schematic representations of
simplified protocol for isolation and purification of antialgal
secondary metabolites have shown in Figure 1 and Figure 2. The
antialgal secondary metabolites isolated from marine macroalgae
have been listed in Table 4, and some possible antialgal compounds
which no final determination has yet been made in the antialgal
components have also been included in the list above. Even if
there is no direct evidence, it is probable that the high diversity of
antialgal secondary metabolites isolated from marine macroalgae.
Furthermore, Tables 5-6 have given EC50-96 h or IC50-96 h, which
are important parameters for controlling red tide microalgae in the
future, of minority antialgal secondary metabolites listed in Table
4 for red tide microalgae.
Quantitative criterion of toxicity of compounds in the inhibitory
experiments of algae growth is as follows: extremely high toxic,
EC50-96 h< 1 µg/mL; high toxic, EC50-96h for 1-10 µg/mL; medium
toxicity, EC50-96 h for 10-100 µg/mL; low toxicity, EC50-96 h>100
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Sun et al.
EC50 of Antialgal Secondary Metabolites
3, 7, 11, 15-tetramethyl-2-hexadecen-1-ol (9.50)
8-hexadecenol (10.6)
(-)-dihydromenisdaurilide (0.240)
3, 7, 11, 15-tetramethyl-2-hexadecen-1-ol (10.5)
Isophytol (1.50)
8-hexadecenol (0.130)
Trehalose (3.27)
twenty-two methyl carbonate (0.620)
17-hydroxyheptadecanoic acid (4.15)
Trans-asarone (3.25)
2-amino-3-mercaptopropanoic acid (1.47)
Trehalose (18.1)
(-)-dihydromenisdaurilide (12.0)
Isophytol (15.0)
17-hydroxyheptadecanoic acid (2.02)
Trans-asarone (15.3)
Twenty-two methyl carbonate (15.5)
3, 7, 11, 15-tetramethyl-2-hexadecen-1-ol (3.32)
8-hexadecenol (7.50)
17-hydroxyheptadecanoic acid (5.46)
Trans-asarone (27.5)
2-amino-3-mercaptopropanoic acid (26.1)
17-hydroxyheptadec Twenty-two methyl (16.6)
Carbonate anoic acid (18.3)
Trans-asarone (19.7)
2-amino-3-mercaptopropanoic acid (14.3)
1, 2-benzenedicarboxylic acid, butyl 2-methylpropyl ester (3.95)
1, 2-benzenedicarboxylic acid, bis(2-methylpropyl) ester (14.0)
µg/mL, according to the literature (OECD, 1984). It’s easy to
found these antialgal secondary metabolites with extremely
high or high toxic against red tide microalgae, including
(-)-dihydromenisdaurilide, 1-O-palmitoyl 2-O-palmitoleoyl-3-
O-β-D-galactopyranosyl glycerol, 7, 10-epoxy-ar-bisabol-11-ol,
gossonorol, and etc. That alone is not enough for determining
their usability in control of red tide microalgae.
Potassium dichromate is a commonly used positive control in
the inhibition experiments of algae growth. So, by comparing
EC50-96 h or IC50-96 h values, it has shown that some antialgal
secondary metabolites have the better application potential
than potassium dichromate as an algal inhibitor against red tide
microalgae in some recent studies (Sun et al., 2016; Sun et al.,
2017; Sun et al., 2018c).
To get more accurate information, this paper classified the results
of these studies for specific red tide microalgae. All antialgal
secondary metabolites obviously better than potassium dichromate
 A Comprehensive Review of Secondary Metabolites with Antialgal Activity from Marine Macroalgae against Red Tide Microalgae483

Table 6. EC50-96 h or IC50-96 h (µg/mL) of antialgal secondary metabolites isolated from marine red macroalgae and brown macroalgae for red tide microalgae.

Red Tide Microalgae EC50 or IC50 of Antialgal Secondary Metabolites

1-O-palmitoyl-3-O-β-D-galactopyranosyl glycerol (IC50=40.5)

1-O-palmitoyl 2-O-palmitoleoyl-3-O-β-D-galactopyranosyl glycerol (IC50=26.4)
a
G. lemaneiformis S. costatum 1-O-palmitoyl-2-O-oleoyl-3-O-β-D-galactopyranosyl glycerol (IC50=41.5)
Uridine (IC50=30.4)
8-hydroxy-4E, 6E-octadien-3-on (IC50=20.6)
b
G. lemaneiformis S. costatum 3β-hydroxy-5α, 6α-epoxy-7-megastigmen-9-one (IC50=147.6)
Stigmasterol (EC50=32)
A. carterae Gossonorol (EC50=1.7)
7, 10-epoxy-ar-bisabol-11-ol (EC50=3.7)
Stigmasterol (EC50=1.7)

15-hydroxymethyl-2, 6, 10, 18, 22, 26, 30-heptamethyl-14-methylene-17-hentriacontene

H. akashiwo (EC50=2.0)

4-hydroxyphenethyl alcohol (EC50=2.2)

Margaric acid (EC50=1.5)
15-hydroxymethyl-2, 6, 10, 18, 22, 26, 30-heptamethyl-14-methylene-17-hentriacontene
(EC50=6.2)
K. mikimitoi
Gossonorol (EC50=3.0)
Stigmasterol (EC50=3.0)
c
G. lemaneiformis 15-hydroxymethyl-2, 6, 10, 18, 22, 26, 30-heptamethyl-14-methylene-17-hentriacontene
(EC50=3.8)
P. globosa
4-hydroxyphenethyl alcohol (EC50=12)
Margaric acid (EC50=4.3)
Gossonorol (EC50=5.1)
P. donghaiense
Glycerol monopalmitate (EC50=4.8)
Gossonorol (EC50=13)

15-hydroxymethyl-2, 6, 10, 18, 22, 26, 30-heptamethyl-14-methylene-17-hentriacontene

S. costatum (EC50=10.4)

4-hydroxyphenethyl alcohol (EC50=16.5)

Margaric acid (EC50=8.7)
Gossonorol (EC50=1.7)
H. akashiwo
7,10-epoxy-ar-bisabol-11-ol (EC50=3.7)
K. mikimitoi 7,10-epoxy-ar-bisabol-11-ol (EC50=1.5)
P. yezoensis P. globosa Gossonorol (EC50=3.0)
P. donghaiense Gossonorol (EC50=5.1)
Ochrophyta
Di (2-ethylhexyl) phthalate (EC50=7864.17)?
L. japonica S. costatum Diisobutyl phthalate (EC50=82.27)?
Cyanoacetylurea (EC50=45086.92)?
Note: a. see reference (Lu, 2011); b. see reference (Sun et al., 2017; Sun et al., 2018b).

(Hoang, O’Leary, and Fotedar, 2016), which EC50-96 h is significantly Cluster View of Macroalgae and Red Tide
lower than that of potassium dichromate, are listed in Table 7. As this paper concluded above, former research works have
This summary provides good reference for the development of been conducted result in some fruits. However, this is far from
environment-friendly algae inhibitors for red tide microalgae. enough for biological control of red tide microalgae using antialgal

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 484 Sun et al.

Table 7. Antialgal secondary metabolites better than potassium dichromate for red tide microalgae.

Red Tide Microalgae Antialgal Secondary Metabolites References

Glycerol monopalmitate, 9-Hexadecenoic acid, 2, 3-dihydroxypropyl ester,

zeaxanthin, pyrrolopiperazine-2, 5-dione, (-)-Dihydromenisdaurilide, 3, 7, 11, Sun et al., 2016; Sun et al., 2017; Sun et
H. akashiwo
15-tetramethyl-2-hexadecen-1-ol, isophytol, 8-hexadecenol, gossonorol, 7, al., 2018c
10-epoxy-ar-bisabol-11-ol, 4-hydroxyphenethyl alcohol
Trehalose, isophytol, 17-Hydroxyheptadecanoic acid, trans-asarone, 2-amino- Sun et al., 2016; Sun et al., 2017; Sun et
K. mikimitoi
3-mercaptopropanoic acid, 7, 10-epoxy-ar-bisabol-11-ol al., 2018c
Glycerol monopalmitate, 1-O-octadecanoic acid-3-O-β-D- galactopyranosyl
glycerol, 1-O-palmitoyl-2-O-oleoyl-3-O-β-D-galactopyranosyl
glycerol, zeaxanthin, pyrrolopiperazine-2, 5-dione, twenty-two methyl Sun et al., 2016; Sun et al., 2017; Sun et
P. globosa
carbonate, 3, 7, 11, 15-tetramethyl-2-hexadecen-1-ol, 8-hexadecenol, al., 2018c
17-Hydroxyheptadecanoic acid, trans-asarone, 2-amino-3-mercaptopropanoic
acid, gossonorol, 4-hydroxyphenethyl alcohol
1-O-octadecanoic acid-3-O-β-D- galactopyranosyl glycerol, 9-Hexadecenoic Sun et al., 2016; Sun et al., 2017; Sun et
P. donghaiense
acid, 2, 3-dihydroxypropyl ester, 17-Hydroxyheptadecanoic acid, gossonorol al., 2018c
S. costatum Glycerol monopalmitate, cholest-5-en-3-ol, pyrrolopiperazine-2, 5-dione Sun et al., 2016

Figure 3. Cluster view of marine macroalgae and red tide in 1998-2018
year.
secondary metabolites isolated from some macroalgae. Therefore,
to give a more explicit knowledge, development relationships
between macroalgae and red tide in the last two decades have
been analyzed by using CiteSpace (Chen, 2009) in this review.
Among these development relationships, this is very clear
that allelopathic interaction (# 1) between macroalgae and red
tide microalgae has been developed into an area during the
last twenty years (Figure 3). However, it is a great pity that
researches on screening, isolation and activity evaluation of
antialgal secondary metabolites are too little in this field so far
(Guo et al., 2017). Therefore, it is urgent for researchers to screen
and isolate antialgal secondary metabolites from more species of
marine macroalgae.
DISCUSSION
In the course of a series of explorations by scientists, a series
of exciting results have been achieved in the studies about growth
inhibition between macroalgae and marine microalgae (Alamsjah
et al., 2005; Bie et al., 2011; Chai, 2016; Chowdhury et al., 2014;
Hirao et al., 2012; Jeong et al., 2000; Jin, Dong, and Wang, 2005;
Lu et al., 2008; Manilal et al., 2010; Nan, Zhang, and Dong, 2004;
Nan, Zhang, and Zhao, 2004; Oh et al., 2010; Pramitha et al.,
2011; Tian, 2009; Wang, Tang, and Sun, 2008; Wang, Xu, and
He, 2007; Wu, 2017; Xu, Qian, and Jiao, 2005; Yu, Lu, and Yang,
2010, and etc.), which provides a new research methods, research
ideas and development directions for red tide biological control
(Table 1, Table 2 and Table 3). At present, it has been confirmed
that some secondary metabolites produced from macroalgae are
the main cause of this growth inhibition (Bie et al., 2011; Hirao
et al., 2012; Kim et al., 2006; Lu, 2011; Ohsawa et al., 2001; Sun
et al., 2015; Sun et al., 2016; Sun et al., 2017; Sun et al., 2018a,
b, c). Macroalgae release some metabolites with antialgal activity
into the environment through infiltration, volatilization and
secretion, etc. These metabolites secreted mainly include phenolic
acids (Sun et al., 2015), alkaloids (Sun et al., 2015), fatty acids
(Alamsjah et al., 2005; Jin, 2005; Oh et al., 2010; Suzuki et al.,
2001), glycolipids (Hirao et al., 2012; Lu, 2011; Sun et al., 2016),
terpenoids (Lu, 2011; Sun et al., 2018a), and others compounds
(An et al., 2008; Bie et al., 2011; Kim et al., 2006; Lu, 2011;
Ohsawa et al., 2001) (Table 4).
Original research articles and publications on overview of
secondary metabolites related to macroalgae are available, but
a supportive systematic review account highlighted secondary
metabolites with antialgal activity is not nearly enough (Tables
5-7; Figure 1 and Figure 2). And what are the development
relationships between macroalgae and red tide microalgae? What
are the research hotspots of the interaction between them? At
present, no reports have been reported. This paper first reported
that the development relationships between macroalgae and red
tide and cluster view of macroalgae and red tide using CiteSpace.
And it clearly pointed out that isolation and purification of
secondary metabolites with antialgal activity produced from
macroalgae are focus of the research in future (Figure 3).

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 A Comprehensive Review of Secondary Metabolites with Antialgal Activity from Marine Macroalgae against Red Tide Microalgae485
CONCLUSIONS
Recent studies on controlling red tide microalgae have mostly
focused on the use of chemical, physical and biological agents,
but these processes have shown some negative environmental
consequences, such as cause secondary pollution (Park et al.,
2013; Rounsefell and Evans, 1958). A variety of extracts from
marine macroalgae containing various bioactive ingredients were
tested. They have wide application range and high antialgal or
algaecides activities (Jeong et al., 2000; Sun et al., 2018a, b,
c; Suzuki et al., 2001; Tang et al., 2015). However, most of the
bioactive compounds extracted from marine macroalgae have
been applied to their biological (antifungal, anti-bacteria) and
drug activities (Zerrifi et al., 2018). There are relatively few
reports about its antialgal or killing activity to red tide microalgae.
To explore macroalgae as a source of environmental friendly
algae inhibitor or algaecide, researchers suggest focusing on new
natural products extracted from marine macroalgae (Ben et al.,
2017).
Some researches have shown that different marine macroalgae
can reduce the proliferation of red tide species and have relatively
low adverse effects on the environment (Jeong et al., 2000; Tang
et al., 2015). There has been an increasing focus on the prospect
of exploiting marine macroalgae as an alternative strategy for
controlling red tide microalgae. The inhibitory properties of
marine macroalgae are mainly due to the release of the bioactive
molecules which mainly are secondary metabolites. The most
well-known molecules are terpenoids, glycerolipids, and various
others secondary compounds (Table 4). Exploiting secondary
metabolites with antialgal activity of marine macroalgae as a
promising alternative to control red tide microalgae evokes a new
prospect.
ACKNOWLEDGMENTS
This work was supported by Special Foundation for Excellent
Young Teachers and Principals Program of Jiangsu Province,
China, the Priority Academic Program Development of Jiangsu
Higher Education Institutions, Postgraduate Research & Practice
Innovation Program of Jiangsu Province (SJCX18_0938), and
the project of Jiangsu key laboratory of marine biotechnology of
Huaihai Institute of Technology of China (HS16004).
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