Distribution, Contents, and Types of Mycosporine-Like Amino Acids (Maas) in Marine Macroalgae and a Database for Maas Based on These Characteristics

marine drugs

Review Distribution, Contents, and Types of Mycosporine-Like Amino Acids (MAAs) in Marine Macroalgae and a Database for MAAs Based on These Characteristics

Yingying Sun 1,2,3,*, Naisheng Zhang 1, Jing Zhou 4, Shasha Dong 1, Xin Zhang 1, Lei Guo 1,2 and Ganlin Guo 2

1 State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi 214122, China; [email protected] (N.Z.); [email protected] (S.D.); [email protected] (X.Z.); [email protected] (L.G.) 2 Jiangsu Key Laboratory of Marine Bioresources and Eco-Environment, Jiangsu Ocean University, Lianyungang 222005, China; [email protected] 3 A Co-Innovation Center of Jiangsu Marine Bio-industry Technology, Lianyungang 222005, China 4 Lianyungang of Products Quality Supervision and Inspection, Lianyungang 222006, China; [email protected] * Correspondence: [email protected]; Tel.: +86-518-85895430

Received: 27 November 2019; Accepted: 1 January 2020; Published: 7 January 2020

Abstract: Mycosporine-like amino acids (MAAs), maximally absorbed in the wavelength region of 310–360 nm, are widely distributed in algae, phytoplankton and microorganisms, as a class of possible multi-functional compounds. In this work, based on the Web of Science, Springer, Google Scholar, and China national knowledge infrastructure (CNKI), we have summarized and analyzed the studies related to MAAs in marine macroalgae over the past 30 years (1990–2019), mainly focused on MAAs distribution, contents, and types. It was confirmed that 572 species marine macroalgae contained MAAs, namely in 45 species of Chlorophytes, 41 species of Phaeophytes, and 486 species of Rhodophytes, and they respectively belonged to 28 orders. On this basis, we established an open online database to quickly retrieve MAAs in 501 species of marine macroalgae. Furthermore, research concerning MAAs in marine macroalgae were analyzed using CiteSpace. It could easily be seen that the preparation and purification of MAAs in marine macroalgae have not been intensively studied during the past 10 years, and therefore it is necessary to strengthen the research in the preparation and purification of MAA purified standards from marine macroalgae in the future. We agreed that this process is not only interesting, but important due to the potential use of MAAs as food and cosmetics, as well as within the medicine industry.

Keywords: CiteSpace analysis; marine macroalgae; mycosporine-like amino acids; online database for MAAs; photoproduction

1. Introduction MAAs (mycosporine-like amino acids) are natural compounds with low molecular weight and exist in diverse aquatic organisms, from algae [1–7] to phytoplankton [2,7–12], cyanobacteria [2,7,13–15], microorganisms [16,17], and marine animals [18–21]. MAAs have maxima absorption ranging between 310 and 360 nm [22]. They constitute a class of more than 30 related UV-absorbing compounds with molecules constituted by imino-carbonyl derivatives of mycosporine cyclohexenone chromophore [7,23]. MAAs exhibited the scavenging eﬀects of oxygen free radicals [24,25], anti-lipid oxidation activity [26], a regulatory role in plant growth

Mar. Drugs 2020, 18, 43; doi:10.3390/md18010043 www.mdpi.com/journal/marinedrugs Mar. Drugs 2020, 18, 43 2 of 23 and development [27], and so on [28]. Meanwhile, MAAs may also possess many physiological functions, including the protection of antitumor activity [29], embryonic and larval development [30], reproduction regulation [23], and osmotic regulation [31]. MAAs were found in marine organisms in the 1960s [17]. However, research pertaining to MAAs in marine macroalgae gradually attracted the attention of researchers in the 1990s [32–34]. More exactly, most studies concerning MAAs in marine macroalgae focused on the period of 1998–2009 [2,4,5,7,35,36]. During this period, MAAs in more than 300 species of marine macroalgae were determined, for example, the green algae Acrosiphonia arcta [4], Boodlea composite [5], Prasiola crispa ssp. antarctica [3], Prasiola crispa [35] and others macroalgae [4,5,7] in Chlorophyta; a class of the brown algae in Phaeophyta, Ecklonia radiata [37], Halopteris scoparia [4], Hydroclathrus clathratus [5], Laminaria saccharina [38], and others brown algae [4,5,7]; many red algae of Rhodophyta, Ahnfeltiopsis devoniensis [39], Apophlaea lyallii [37], Bangia atropurpurea [40], Chondrus crispus [41], Gracilaria chilensis [42], Iridaea sp. [43], Palmaria palmata [44], Porphyra umbilicalis [1] and etc. [4,5,7,45,46]. From 2009 to 2019, MAAs in less than 200 species, such as Bangia atropurpurea [47], Calliarthron tuberculosum [48], Catenella repens [49], Gelidium lingulatum [50], Gloiopeltis furcate [51], Palmaria palmata [52], Pyropia plicata [53], Solieria chordalis [54] and others macroalgae [55–58], were found. Marine macroalgae as marine primary productivity have developed complex and unique metabolic pathways. Therefore, they have been become the target of exploiting natural bioactive components. To date, MAAs in more than 500 marine macroalgae have been reported. However, unfortunately, the summary and generalization about these researches were lacked. This made it very difficult to provide relevant information on MAAs of marine macroalgae. Therefore, this paper will provide an overview of MAAs in marine macroalgae since 1990 and focus on the contents and types of MAAs, and their distribution in marine macroalgae. The two databases related MAAs in marine macroalgae have been showed [2,59]. Although these two databases were not specific databases for MAAs in marine macroalgae, and provide less information regarding MAAs, the lack of total MAAs contents and specific MAA content, these works provided us with a good idea. Therefore, further in paper we established an open online database for MAAs in 501 species of marine macroalgae to quickly retrieve some related information regarding MAAs in marine microalgae since 1990. A lot of information, such as the source (field/culture) and collection site of marine macroalgae, the total MAAs contents, specific MAA content, and/or MAAs composition etc., were included in this online database (http://210.28.32.218/MAAs/). CiteSpace was a software used in scientific literature to identify and display new trends of scientific development [60]. Finally, in this review, the development tendency of the studies about MAAs in marine macroalgae will be analyzed using CiteSpace to point out future research directions for researchers in related fields. This is not only very interesting, but also can promote the development of MAAs in marine macroalgae.

2. Results

2.1. MAAs Distribution, Contents and Types in Marine Macroalgae In our survey that summarized of more than 660 species, 572 species of marine macroalgae contained MAAs, found namely in 45 species in Chlorophyta, 41 species in Phaeophyta, and 486 species in Rhodophyta (Figure1), and they respectively belonged to 28 orders (Figure2). Among them, marine macroalgae which contained MAAs mainly distributed in orders Bangiales, Ceramiales, Gigartinales, and Gracilariales. MAAs rfepresent a class of the secondary metabolites in marine macroalgae [61,62], and in addition to antioxidant [24–28] and anti-ultraviolet radiation activities [22,23,63], likely possess many physiological activities, such as capacity to inhibit the proliferation of tumor cells [29], protecting embryonic and larval development [30], and regulating reproduction [23] and osmosis [31]. The research eﬀorts made pertaining to MAAs in marine macroalgae have drawn signiﬃcant attention since 1990. The contents and composition of MAAs in marine macroalgae were important Mar. Drugs 2020, 18, 43 3 of 23

Mar. Drugs 2020, 18 FOR PEER REVIEW 3

Mar. Drugs 2020, 18 FOR PEER REVIEW 3 in developingcomposition MAAs. in marine Therefore, macroalgae the have summary been conducted and analysis according of totalto different MAAs orders contents in this and paper MAAs composition in marine macroalgae have been conducted according to diﬀerent orders in this paper (Figurescomposition 2–4). in marine macroalgae have been conducted according to different orders in this paper (Figures2–4). (Figures 2–4). 45

45 41 41

Chlorophyta

PhaeophytaChlorophyta RhodophytaPhaeophyta Rhodophyta

486 486 Figure 1. Distribution of MAAs in different phylums of marine macroalgae. Data extracted from Figurerelated 1. Distribution studies since of MAAs1990, and in ditheﬀerent number phylums in a pi ofe marinechart represents macroalgae. the total Data number extracted of frommarine related Figure 1. Distribution of MAAs in different phylums of marine macroalgae. Data extracted from studiesmacroalgae since 1990, species and belong the number to this phylum. in a pie chart represents the total number of marine macroalgae related studies since 1990, and the number in a pie chart represents the total number of marine species belong to this phylum. macroalgae species belong to this phylum.

1 3 2 4 12 11 6 1 3 2 2 60 8 4 11 27 12 6 6 2 60 9 8 6 1 9 27 6 9 6 1 9 16

52 136

97 9 32 97 5 9 28 5 11 8 5 32 5 28 5 11 8 5

FigureFigure 2. Distribution 2. Distribution of MAAsof MAAs in in di differentfferent ordersorders of marine marine macroalgae. macroalgae. Data Data extracted extracted from from related related studiesstudies since since 1990, 1990, and and the the number number in in a a pie pie chartchart representsrepresents the the total total number number of marine of marine macroalgae macroalgae Figure 2. Distribution of MAAs in different orders of marine macroalgae. Data extracted from related speciesspecies belong belong to this to this order. order. The The several several highlights highlights parts in in the the pie pie chart chart are are just just for forclarity. clarity. studies since 1990, and the number in a pie chart represents the total number of marine macroalgae species belong to this order. The several highlights parts in the pie chart are just for clarity. MAAsMAAs have have been been found found in in 45 45 species species ofof thethe greengreen algae algae in in Chlorophyta Chlorophyta [2–5,7,35,64]. [2–5,7,35, 64Among]. Among them,them, total total MAAsMAAs MAAs have contents contents been werefound were determinied in determinied 45 species of inin the onlyonly green 12 12 species. species.algae in The Chlorophyta The green green algae algae[2–5,7,35,64]. with with high high totalAmong total MAAsMAAs contentsthem, contents total belong MAAs belong to contents Prasiolales,to Prasiolales, were and anddeterminied contents contents werein on morely more 12 thanspecies. than 3.5 3.5 mg/gThe mg green DW/g DW (Figure algae (Figure with3a), 3such a),high such as total as PrasiolaPrasiola crispaMAAs crispassp. contents ssp.antarctica antarctica belong[3 ],to [3],Prasiola Prasiolales, Prasiola crispa crispa andcollected contentscollected from were from South more South than Shetlands Shetlands 3.5 mg/g [ [40]40 DW] andand (Figure KongsfjordenKongsfjorden 3a), such [as35 ] [35] respectively. The total MAAs contents in other macroalgal Chlorophytes were very low, with respectively.Prasiola The crispa total ssp. MAAs antarctica contents [3], Prasiola in other crispa macroalgal collected from Chlorophytes South Shetlands were [40] very and low, Kongsfjorden with values values ranging between 0.0045 and 0.275 mg/g DW. Therefore, some bars which represent the total ranging[35] between respectively. 0.0045 The and total 0.275 MAAs mg/g contents DW. Therefore, in other macroalgal some bars Chlorophytes which represent were thevery total low, MAAswith MAAs contents in different marine Chlorophytes were almost on the ordinate. contentsvalues in diff rangingerent marine between Chlorophytes 0.0045 and 0.275 were mg/g almost DW. on Therefore, the ordinate. some bars which represent the total MAAsThe brown contents algae in different (41 species) marine in Chlorophytes Phaeophyta werealso almostwere confirmedon the ordinate. to contain MAAs [2– The brown algae (41 species) in Phaeophyta also were confirmed to contain MAAs [2–5,32,37,38] 5,32,37,38]The (Table brown 1). Further,algae (41 for species) eight species, in Phaeophyta namely Chorda also tomentosa were confirmed [4], Desmarestia to contain menziesii MAAs [32], [2– (Table1). Further, for eight species, namely Chorda tomentosa [4], Desmarestia menziesii [32], Dictyota Dictyota5,32,37,38] bartayresii (Table [5], 1). Further,Dictyosiphon for eight foeniculaceus species, namely [4], Pilayella Chorda tomentosalittoralis [4],[4], DesmarestiaEcklonia radiata menziesii [37], [32], bartayresiiDictyota[5], Dictyosiphon bartayresii [5], foeniculaceus Dictyosiphon [foeniculaceus4], Pilayella [4], littoralis Pilayella[4 ],littoralisEcklonia [4], radiata Ecklonia[37 radiata], Halopteris [37], scoparia [4], Hydroclathrus clathratus [5] and Sargassum oligocystum [5], the total MAAs contents were pointed out. These values were very low and less than 0.2 mg/g DW (Figure3b). Mar. Drugs 2020, 18 FOR PEER REVIEW 4

Halopteris scoparia [4], Hydroclathrus clathratus [5] and Sargassum oligocystum [5], the total MAAs Mar. Drugs 2020, 18, 43 4 of 23 contents were pointed out. These values were very low and less than 0.2 mg/g DW (Figure 3b). A total of 486 MAA-containing strains of macroalgal Rhodophytes were detected. In order to presentA total these of 486 reports MAA-containing from 1990 strainsto 2019 of more macroalgal clearly, Rhodophytes they are shown were detected.in two maps In order in Figure to present 3c,d, thesewith reports 2009 as from the 1990 cut-off to 2019 time more point. clearly, Among they them, are shown the total in two MAAs maps contents in Figure 3inc,d, 323 with red 2009 algae as thewere cut-offdetermined, time point. and Amongtheir MAAs them, contents the total were MAAs usually contents higher in 323compared red algae with were macroalgal determined, Chlorophytes and their MAAsand Phaeophytes contents were [2–5,40,65]. usually higher For comparedexample, withsome macroalgal members Chlorophytesof orders Bangiales and Phaeophytes [5,40,65], Gracilariales[2–5,40,65]. For[3,32,66], example, Gigartinales some members [5,40,42], of orders and Gelidiales Bangiales [[48,5,4067],,65], their Gracilariales total MAAs[3,32 contents,66], Gigartinales ranges from [5,40 2 ,mg/g42], andDW Gelidiales to nearly [2048 ,67mg/g], their DW. total Of course, MAAs there contents were ranges also many from 2macroalgal mg/g DW Rhodophytes to nearly 20 mgwith/g lower DW. Oftotal course, MAAs there contents, were also such many as Actinotrichia macroalgal fragilis Rhodophytes [5], Asparagopsis with lower taxiformi total MAAs[5], Galaxaura contents, oblongata such as[5],Actinotrichia Gelidium corneum fragilis [[68],5], Asparagopsis and Georgiella taxiformi confluens[5 ],[3],Galaxaura etc. [3–5,69], oblongata and these[5], Gelidium values were corneum even[68 less], andthanGeorgiella 0.1 mg/g confluens DW. Further,[3], etc. we [3 –classified5,69], and these these re valuesd algae were into even three less groups than 0.1according mg/g DW. to their Further, total weMAAs classified contents. these redThe algae first into group, three groupsincluding according 65 species to their belong total MAAsto order contents. Balliales, The firstCeramiales, group, includingCorallinales, 65 species Nemaliales belong and to order Rhodymeniales, Balliales, Ceramiales, exhibited Corallinales, low total MAAs Nemaliales contents and (< Rhodymeniales, 1 mg/g DW). A exhibitedsecond group low total with MAAs the higher contents concentratio (< 1 mg/gn DW). of total A second MAAs group and 52 with species the highershowed concentration 1～2 mg/g DW of totalMAAs. MAAs The and last 52 speciesgroup showedthat included 1~2 mg 216/g DW species, MAAs. such The as last the group orders that includedBangiales, 216 Gelidiales, species, suchGigartinales, as the orders and Bangiales, Gracilariales Gelidiales, macroalgae Gigartinales, showed and the Gracilariales highest total macroalgae MAAs showedcontents the and highest these totalvalues MAAs are contentsall above and2 mg/g these DW. values Of note, are all Rhodymenia above 2 mg spp./g DW.Belonging Of note, to Rhodymeniaorder Rhodymenialesspp. Belonging had a tosurprisingly order Rhodymeniales high MAAs had contents a surprisingly (8.8–142.9 high mg/g MAAs DW, contents average (8.8–142.9 value 75.85 mg mg/g/g DW, DW) average [37]. valueThis is 75.85clearly mg displayed/g DW) [37 in]. Figure This is 2c clearly with displayedanother axe in (maximum Figure2c with value another of abscissa axe (maximum 80). In addition, value of the abscissaMAAs 80).content In addition, value thein MAAseach contentmarine valuemacroalgae in each marinecould macroalgaebe obtained could using be obtained the database using the(http://210.28.32.218/MAAs/) database (http://210.28.32.218 built/MAAs by our/) built team by, which our team, we will which explain we will in detail explain later. in detail later.

Concentration of MAAs (mg/g DW)

00.511.522.533.544.5

Ulvales (11) Ulotrichales (4) Siphonocladales (3) Prasiolales (6) Dasycladales (5)

MAAs in Chlorophytes in MAAs Cladophrales (9) Bryopsidales (6) Class of marine Class of marine macroalgae contained 0 0.1 0.2 0.3

Concentration of MAAs (mg/g DW)

(a)

Sphacelariales (2)

Scytosiphonales (1)

Laminariales (9)

Fucales (11)

Ectocarpales (8)

Dictyotales (5) MAAs in Phaeophytes in MAAs

Desmarestiales (5) Order of marine Order of marine macroalgae contained 0 0.05 0.1 0.15 0.2

Concentration of MAAs (mg/g DW) (b)

Figure 3. Cont.

Mar. Drugs 2020, 18, 43 5 of 23 Mar. Drugs 2020, 18 FOR PEER REVIEW 5

Concentration of MAAs (mg/g DW) 0 20406080 Rhodymeniales (7) Plocamiales (7) Palmariales (20) Nemaliales (6) Hildenbrandiales (1) Halymeniales (14) Gracilariales (25) Gigartinales (57) Gelidiales (15) Corallinales (19) Ceramiales (103) Bonnemaisoniales (4) Bangiales (41)

from Rhodophytesfrom 2009 to 1990 from Balliales (2)

Order of marine Order of marine macroalgae contained MAAs 0 2 4 6 8 101214161820

Concentration of MAAs (mg/g DW) (c)

Concentration of MAAs (mg/g DW) 0 2 4 6 8 10 12 14 16 Rhodymeniales (5) Plocamiales (1) Palmariales (7) Nemaliales (3) Halymeniales (2) Gracilariales (27) Gigartinales (40) Gelidiales (13) Corallinales (13) Ceramiales (33) Bonnemaisoniales (2) Bangiales (19) from Rhodophytes between 2009 and 2019 and 2009 between Rhodophytes from

Order of marine Order of marine macroalgae contained MAAs 0 2 4 6 8 10 12 14 16

Concentration of MAAs (mg/g DW) (d)

FigureFigure 3.3. TheThe contentscontents ofof totaltotal MAAsMAAs inin didifferentfferent ordersorders ofofmarine marinemacroalgae. macroalgae. DataData extractedextracted fromfrom relatedrelated studiesstudies since since 1990. 1990. The The number number in bracketin bracket represents represents the number the number of species of species included included in orders, in barorders, represents bar represents a marine a macroalgaemarine macroa withlgae corresponding with corresponding MAAs in MAAs (a–d), andin (a the–d), bars and withthe bars different with widthsdifferent represent widths therepresent numbers the of numbers some marine of some macroalgae marine macroalgae with corresponding with corresponding MAAs in (c,d MAAs). in (c,d). From 1990 to 2019, the survey found that MAAs in marine macroalgae mainly focus on macroalgal RhodophytesFrom 1990 (Figure to 2019,1), therefore, the survey MAAs found types that in RhodophytesMAAs in marine have beenmacroalgae pointed outmainly according focus toon dimacroalgalfferent orders Rhodophytes of macroalgal (Figure Rhodophytes 1), therefore, in this MA reviewAs types (Figure in Rhodophytes4). Identified have MAAs been in macroalgalpointed out Rhodophytesaccording to different included orders 22 types, of macroalgal namely AplysiapalythineRhodophytes in this A, review Aplysiapalythine (Figure 4). Identified B, asterina-330, MAAs catenelline,in macroalgal mycosporine-alanine-glycine, Rhodophytes included 22 mycosporine-glycine, types, namely Aplysiapalythine mycosporine-methylamine-threonine, A, Aplysiapalythine B, mycosporine-2-glycine,asterina-330, catenelline, palythene, palythenicmycosporine-alanine-glycine, acid, palythinol, porphyra-334, mycosporine-glycine, palythine, shinorine, usujirene,mycosporine-methylamine-threonine, and new MAAs prasiolin [70mycosporine-2-glycine,] and bostrychines A–F [palythene,71]. Among palythenic them, shinorine, acid, porphyra-334,palythinol, porphyra-334, palythine and palythine, asterina-330 shinorine, were more usujirene, abundant, and followed new MAAs by palythinol; prasiolin catenelline, [70] and mycosporine-2-glycine,bostrychines A–F [71]. Among mycosporine-methylamine-threonine them, shinorine, porphyra-334, palythine and palythenic and asterina-330 acid were were very more few. Amongabundant, them, aplysiapalythinefollowed A,by aplysiapalypalythinol; thine B, catenelline,catenelline, and novelmycosporine-2-glycine, MAAs (prasiolin and bostrychinesmycosporine-methylamine-threonine A–F) were only found in macroalgaland palythenic Rhodophytes acid [49were,70– 72very]. Moreover, few. Among it is noted them, that MAAsaplysiapalythine have not yet A, been aplysiapaly identified thine in many B, catenellin species ofe, and macroalgal novel MAAs Rhodophytes, (prasiolin and and therefore bostrychines it is quite A– possibleF) were only that newfound MAAs in macroalgal will be discovered Rhodophytes from [49, those70–72]. macroalgae. Moreover, Seven it is MAAs, noted that such MAAs as asterina-330, have not yet been identified in many species of macroalgal Rhodophytes, and therefore it is quite possible that new MAAs will be discovered from those macroalgae. Seven MAAs, such as asterina-330,

Mar.Mar. Drugs Drugs 20202020,, 1818 ,FOR 43 PEER REVIEW 6 of 236 mycosporine-glycine, palythene, palythinol, porphyra-334, palythine, and shinorine were found in macroalgalmycosporine-glycine, Chlorophytes palythene, and Phaeophytes, palythinol, however porphyra-334, other palythine,types MAAs and have shinorine not been were found found in in themmacroalgal except Chlorophytes for unidentified and MAAs. Phaeophytes, These howeverresults can other be queried types MAAs through have the not database been found mentioned in them above.except for unidentiﬁed MAAs. These results can be queried through the database mentioned above.

Figure 4. Types of MAAs in macroalgal Rhodophytes. Data extracted from related studies since Figure 4. Types of MAAs in macroalgal Rhodophytes. Data extracted from related studies since 1990, 1990, and the number in a pie chart represents the total number of macroalgal Rhodophyta contained andidentical the number MAA. The in a several pie chart highlights represents parts the in thetotal pie number chart are of just macroalgal for clarity. Rhodophyta contained identical MAA. The several highlights parts in the pie chart are just for clarity. In Figure5, main MAAs in macroalgal Rhodophytes, such as asterina-330, mycosporine-glycine, palythene,In Figure palythinol, 5, main porphyra-334, MAAs palythine,in macroalgal shinorine Rhodophytes, and usujirene, such were listedas asterina-330, according to mycosporine-glycine,different orders. It can palythene, be clearly shown palythinol, that these porphy MAAsra-334, were palythine, common in shinorine marine macroalgae and usujirene, belonging were listedto orders according Ceramiales to different and Gigartinales orders. macroalgae.It can be clearly Further, shown porphyra-334, that these palythine MAAs andwere shinorine common were in marinecommonly macroalgae found in ordersbelonging Bangiales to orders and Gracilariales Ceramiales macroalgae. and Gigartinales And porphyra-334 macroalgae. and shinorineFurther, porphyra-334,were also the most palythine common and inshinorine macroalgal were Chlorophytes commonly found and Phaeophytes, in orders Bangiales but they and usually Gracilariales occurred macroalgae.in lower concentrations. And porphyra-334 Meanwhile, and mycosporine-glycine shinorine were seemedalso the to havemost thecommon highest concentrationin macroalgal in ChlorophytesChlorophytes andand PhaeophytesPhaeophytes, species but they [4,5, 73usually], for example, occurred the in proportion lower concentrations. of mycosporine-glycine Meanwhile, in mycosporine-glycineMAAs for Chlorophytes seemedBoodlea to compositahave the [highest5], Chaetomorpha concentration aerea [in4], ChlorophytesCodium fragile and[73], PhaeophytesEnteromorpha speciesintestinalis [4,5,73],[73], Halimeda for example, polentia the[73 ],proportionRhizoclonium of tortuosummycosporine-glycine[73], Spongomorpha in MAAs spinescens for Chlorophytes[73], and Ulva Boodlealactuca [composita73] is more [5], than Chaetomorpha 53%; in Phaeophytes aerea [4], CodiumAgarum fragile cribosum [73], Enteromorpha[73], Alaria esculenta intestinalis[73 [73],], Ascophyllum Halimeda polentianodosum [73],[73 ],RhizocloniumChorda filum tortuosum[73], Drsmarestia [73], Spongomorpha aculeata [73 ],spinescensElachista [73], fucicola and[ 73Ulva], Fucus lactuca vesiculosis [73] is more[73], thanLaminaria 53%; saccharinain Phaeophytes[73], Laminariocolas Agarum cribosum tomentosoides [73], Alaria[73], andesculentaSargassum [73], fluitansAscophyllum[73], thisnodosum proportion [73], Chordawas higher filum than[73], 87%,Drsmarestia even as aculeata high as [73], 100% Elachista in Alaria fucicola esculenta [73],[ 73Fucus], Elachista vesiculosis fucicola [73],[ 73Laminaria], Fucus saccharinavesiculosis [[73],73], LaminariaLaminariocolas saccharina tomentosoides[73], and Laminariocolas[73], and Sargassum tomentosoides fluitans[73 [73],]. In Rhodophytes,this proportion such was as higherAcanthophora than 87%, specifera even[ as5], highChondrus as 100% crispus in Alaria[73], Corallina esculenta o[73],fficinalis Elachista[73], fucicolaCystoclonium [73], Fucus purpureum vesiculosis[73], [73],Lomentaria Laminaria orcadensis saccharina[73], Mastocarpus[73], and Laminariocolas stellata [73], Phycodrystomentosoides rubens [73].[73 In], PorphyraRhodophytes, umbilicalis such[ 73as], Acanthophoraand other red specifera algae [[5],2–7 ,Chondrus32–35,40, 42crispus–45,55 [73],,69, 71Corallina,74–78], officinalis the proportion [73], Cystoclonium of mycosporine-glycine purpureum [73], in LomentariaMAAs was orcadensis lower than [73], 50%; Mastocarpus and relatively stellata numerous [73], Phycodrys species rubens (more [73], than Porphyra 260 species) umbilicalis did not [73], detect and otherthis MAA, red algae for instance, [2–5,7,32–35,40,42–45,55,69,71,74–79],Actinotrichia fragilis [5], Ahnfeltiopsis the proportion devoniensis of [mycosporine-glycine39], Amphiroa rigida [in2], MAAsAsparagopsis was lower armata than[4 ],50%; and andBangia relatively atropurpurea numerous[3], species etc. [1 –(more5,40–42 than,44, 55260,58 species),65,67–72 did,74 not,76, 79detect–87]. thisHowever, MAA, infor Rhodophytesinstance, ActinotrichiaApophlaea fragilis lyallii [5],[37 ]Ahnfeltiopsis and Palmaria devoniensis palmata [39],[73], Amphiroa the proportion rigida [2], of Asparagopsismycosporine-glycine armata [4], in MAAsand Bangia was very atropurpurea high. Therefore, [3], etc those. [1–5,40–42,44,55,58,65,67–72,74,76,80–88]. Chlorophytes [4,5,73], Phaeophytes [73], However, in Rhodophytes Apophlaea lyallii [37] and Palmaria palmata [73], the proportion of mycosporine-glycine in MAAs was very high. Therefore, those Chlorophytes [4,5,73], Phaeophytes

Mar. Drugs 2020, 18, 43 7 of 23 Mar. Drugs 2020, 18 FOR PEER REVIEW 7 and[73], two and Rhodophytes two Rhodophytes [37,73] species [37,73] mentioned speciesabove mentioned were good above sources were of mycosporine-glycine.good sources of Somemycosporine-glycine. reports have determined Some reports that mycosporine-glycine,have determined that mycosporine-glycine, porphyra-334, and shinorineporphyra-334, have and better antioxidantsshinorine have properties better [29antioxidants,39,88,89], andproperties therefore [29,39,89,90], many macroalgal and therefore Rhodophytes many speciesmacroalgal which belongedRhodophytes to the species orders Bangiales,which belong Ceramiales,ed to the Gigartinales, orders Bangiales, and Gracilariales Ceramiales, have Gigartinales, been considered and toGracilariales constitute prolific have been sources considered of porphyra-334 to constitute and proli shinorine,fic sources e.g., of porphyra-334Acanthophora and specifera shinorine,[5], e.g.,Bangia atropurpureaAcanthophora[65 specifera], Caloglossa [5], Bangia apomeiotica atropurpurea[5], Porphyra [65], Caloglossa dioica [57 apomeiotica], Bostrychia [5], radicans Porphyra[40 dioica], Ceramium [57], nodulosumBostrychia[ 4radicans], Catenella [40], impudica Ceramium[40], nodulosumCurdiea racovitzae [4], Catenella[32], Gracilaria impudica domingensis[40], Curdiea[90 racovitzae], Gymnogongrus [32], griGracilariaffithsiae [ 4],domingensis and Mastocarpus [91], stellatusGymnogongrus[4], etc. grif [3,5fi,thsiae32,40 ,48[4],,50 ,and74,85 ,Mastocarpus91–93]. stellatus [4], etc. [3,5,32,40,48,50,74,85,92–94].

(a) (b)

(e) (f)

Figure 5. Cont.

Mar. Drugs 2020, 18, 43 8 of 23 Mar. Drugs 2020, 18 FOR PEER REVIEW 8

Mar. Drugs 2020, 18 FOR PEER REVIEW 8

(g) (g) (h) (h)

FigureFigure 5. Distribution 5. Distribution of specific of specific MAA inMAA differen in t differenorders oft ordersmacroalgal of macroalgalRhodophytaes. Rhodophytaes. Data Data Figure 5. Distribution(g) of specific MAA in different orders of macroalgal(h) Rhodophytaes. Data extractedextractedextracted fromfrom from related related studies studies studies since since 1990, since 1990, and 1990, the and nuand thember the number in nu amber pie inchart in a piea represents pie chart chart represents the represents total number the the total total numbernumber ofFigure red macroalgae 5. Distribution that contained of specific specific MAA MAA in differen belong tto orders this order. of macroalgal (a), (b), (c), (Rhodophytaes.d), (e), (f), (g) and Data (h) of redof macroalgae red macroalgae that that contained contained specific specific MAA MAA belong belong to to thisthis order. ( (aa),– (hb)), represent (c), (d), (e), specific (f), (g) and MAA (h) representextracted fromspecific related MAA studies Asterina-330, since 1990, Mycosporinand the numbere-glycine, in a pie Palythene, chart represents Palythine, the total Palythinol, number represent specific MAA Asterina-330, Mycosporine-glycine, Palythene, Palythine, Palythinol, Asterina-330,Porphyra-334,of red macroalgae Mycosporine-glycine,Usujirene that contained and Shinorine, specific respectively. Palythene, MAA belong Palythine, to this order. Palythinol, (a), (b), (c), ( Porphyra-334,d), (e), (f), (g) and Usujirene(h) and Porphyra-334, Usujirene and Shinorine, respectively. Shinorine,represent respectively.specific MAA Asterina-330, Mycosporine-glycine, Palythene, Palythine, Palythinol, InPorphyra-334, addition, it Usujireneis worth andmentioning Shinorine, that respectively. the difference of the total MAAs or MAA value between cultivatedIn addition,In marineaddition, it macroalgae is it worth is worth mentioning and mentioning field material that that existed the the di fffromdierencefference same of collection of the the total total location. MAAs MAAs For or or MAAexsample, MAAvalue value betweenbetween cultivatedculturedcultivatedIn addition, marineStictosiphonia marine it macroalgae is worth macroalgaetangatensi mentioning and [40] and field exhibited that field material the material dionlyfference existed47.8% existed of ofthe from the fromtotal total same MAAs same MAAs collection orcollection MAA found valuelocation. inlocation. the between field ForFor exsample, culturedsamplecultivatedculturedStictosiphonia [5]. marine Chondrus Stictosiphonia macroalgae crispus tangatensi , tangatensiwhich and[ 40field in] exhibitedculture material[40] exhibited esposured existed only 47.8% fromonly to green same of47.8% the orcollection total blueof the MAAslight location. total radiation, found MAAs Forin exsample,exhibited thefound field in sample the field [5]. asterina-330,cultured Stictosiphonia palythene, tangatensi palythinol [40] and exhibited shinorine only that 47.8% were of lack the oftotal MAAs MAAs in foundthe field in thesample. field Chondrussample crispus [5]. Chondrus, which in crispus culture, which esposured in culture to green esposured or blue to lightgreen radiation, or blue light exhibited radiation, asterina-330, exhibited Similarysampleasterina-330, [5]. phenomenons Chondrus palythene, crispus also occurr, whichpalythinoled in in culture other and seaweeds, esposured shinorine such to thatgreen as Bostrychia were or blue lack lightradicans of radiation, MAAs [5,40], Caloglossainexhibited the field sample. palythene, palythinol and shinorine that were lack of MAAs in the field sample. Similary phenomenons stipitataasterina-330,Similary [5,49], phenomenons palythene, Chondrus palythinolcrispus also occurr[60,72], and edshinorine Kallymenia in other that seaweeds,antarctica were lack such[3], of Mazzaella MAAsas Bostrychia in laminarioidesthe radicansfield sample. [74],[5,40], Caloglossa alsoNeuroglossumSimilary occurred phenomenons inligulatum other seaweeds, also[3], Palmariaoccurred such decipiensin other as Bostrychia seaweeds,[3], Plocamium radicanssuch ascartilagineum Bostrychia[5,40], Caloglossa radicans[3], Porphyra [5,40], stipitata columbinaCaloglossa[5,49 ], Chondrus stipitata [5,49], Chondrus crispus [60,72], Kallymenia antarctica [3], Mazzaella laminarioides [74], crispus[43,79],stipitata[60 and ,72[5,49], ],PorphyraKallymenia Chondrus endiviifolium antarcticacrispus [3].[60,72], [In3], theMazzaella Kallymeniadatabaselaminarioides that antarctica we set up[3],[ 74later, ],MazzaellaNeuroglossum we made laminarioides clear ligulatumthe source [74], [ 3], Palmaria Neuroglossum ligulatum [3], Palmaria decipiens [3], Plocamium cartilagineum [3], Porphyra columbina decipiensofNeuroglossum marine[3], macroalgaePlocamium ligulatum that cartilagineum[3], was Palmaria field or decipiens [culture,3], Porphyra or[3], commercial Plocamium columbina provision. cartilagineum[6,43], and [3],Porphyra Porphyra endiviifolium columbina [3]. In the [43,79], and Porphyra endiviifolium [3]. In the database that we set up later, we made clear the source database[43,79],The thatand specific Porphyra we set parameters up endiviifolium later, weof [3].10 made typesIn the clear ofdatabase MAAs the source that in wemarine of set marine up macroalgae, later, macroalgae we made such clear thatas thestructure, was source field or culture, extinctionof ofmarine marine macroalgaecoefficient, macroalgae retentionthat wasthat field timewas orfieldand culture, maximum or culture, or commercial absorption or commercial provision. wavelength, provision. have been showed in or commercial provision. TableThe 1. TheUnfortunately, specific specific parameters parameterssome parameters of 10 oftypes 10of thesetypesof MAAs MAAs of MAAs inhave marine not in been macroalgae,marine determined, macroalgae, such for asinstance, structure, such the as structure, extinctionextinctionTheextinction specific coefficientcoefficient, coefficient, parameters ofretention mycosporine-2-glycine retention of time 10types andtime maximum ofand MAAs andmaximum absorptionusujirene. in marine absorption Thiswavelength, macroalgae, should wavelength, behave due such been to as thehaveshowed structure, lack been ofin showed extinction in coecommerciallyTableffiTablecient, 1. Unfortunately, 1. retention Unfortunately, available time MAAssome andsomeparameters standards. maximumparameters of these absorptionof MAAs these have MAAs wavelength,not havebeen determined,not been have determined, for been instance, showed for the instance, in Table the1. Unfortunately,extinctionextinction coefficient somecoefficient parameters of mycosporine-2-glycine of mycosporine-2-glycine of these MAAs and have usujirene. and not usujirene. been This determined,should This be should due for to instance, bethe duelack to theof the extinction lack of Table 1. Structure, molar extinction coefficient, retention time, and maximum absorption coecommerciallyfficommerciallycient of mycosporine-2-glycine available available MAAs MAAs standards. standards. and usujirene. This should be due to the lack of commercially wavelength of MAAs in marine macroalgae [43,95]. available MAAs standards. Table 1. Structure, molar extinction coefficient, retention time, and maximum absorption Table 1. Structure, molar extinction coefficient,Extinction retention time, and maximum absorption wavelength of MAAs in marine macroalgae [43,95]. Maximum Absorption Table 1.MAAStructure, molar extinctionStructure coefficient, retentionCoefficient time, ε and maximum absorption wavelength wavelength of MAAs in marine macroalgae [43,95]. Wavelength (nm) of MAAs in marine macroalgae [43,94]. (MExtinction−1 cm-1) Maximum Absorption MAA Structure CoefficientExtinction ε Wavelength Maximum(nm) Absorption MAA Structure (M−1 cmExtinction-1) Coefficient Coe ε ffi cient Maximum Absorption MAA Structure 1 1 Wavelength (nm) ε (M −1 cm-1 ) Wavelength (nm) (M− cm−) Asterina-330 43,800 330

Asterina-330Asterina-330 43,80043800 330 330

Asterina-330 43,800 330

Mycosporine-2-glycine — 334 Mycosporine-2-glycine — 334

Mycosporine-2-glycine — 334

Mar. Drugs 2020, 18 FOR PEER REVIEW 9

Mar. DrugsMycosporine-glycine 2020, 18 FOR PEER REVIEW 28,100 310 9

Mar. Drugs Mycosporine-glycine2020, 18 FOR PEER REVIEW 28,100 310 9

Mar. Drugs 2020 18 Mar. Drugs Mycosporine-glycine2020, , 18, 43FOR PEER REVIEW 28,100 310 9 9 of 23

Mycosporine-glycine 28,100 310 Table 1. Cont. Palythene 50,000 360 Mycosporine-glycine 28,100 310

Palythene 50,000 360 Mycosporine-glycineMycosporine-glycine 28,10028100 310 310

Palythene 50,000 360

Palythene 50,000 360 Palythine 35,500~36,200 320 PalythenePalythene 50,00050000 360 360

Palythine 35,500~36,200 320 Palythene 50,000 360

Palythine 35,500~36,200 320

PalythinePalythine 35,500~36,20035500~36200 320 320 Palythenic acid 29,200 337

Palythine 35,500~36,200 320 Palythenic acid 29,200 337

Palythine 35,500~36,200 320 PalythenicPalythenic acid acid 29,20029200 337 337

Palythenic acid 29,200 337

Palythinol 43,500 332 Palythenic acid 29,200 337

PalythinolPalythinol 43,500 43500332 332

Palythenic acid 29,200 337

Palythinol 43,500 332

Mar. Drugs 2020, 18 FOR PEER REVIEW 10

Porphyra-334Porphyra-334Palythinol 42,30043,500 42300 334332 334

Mar. Drugs 2020, 18 FOR PEER REVIEW 10 Porphyra-334Palythinol 42,30043,500 334332

Porphyra-334 42,300 334

Shinorine 43,700 334

ShinorinePorphyra-334 42,30043700 334 334

Shinorine 43,700 334

Porphyra-334 42,300 334

Shinorine 43,700 334

Porphyra-334 42,300 334

Shinorine 43,700 334 Usujirene — 357 Usujirene — 357

Shinorine 43,700 334

Usujirene — 357

Shinorine 43,700 334

In order to clearly present the distribution of speciﬁc MAA in each marine macroalgae, based on In order to clearly present the distribution of specific MAA in each marine macroalgae, based theon literature the literature information information from from the the Web Web of of Science, Science, Springer, Springer, Google Google Scholar, Scholar, and andCNKI, CNKI, Tables Tables 2 2 and3 areand presenteed. 3 are presenteed. In these In twothese tables,two tables, all marineall marine macroalgae macroalgae were were groupedgrouped according according to tothe the types of MAAstypesIn that of order MAAs they to that contained.clearly they present contained. the distribution of specific MAA in each marine macroalgae, based on the literature information from the Web of Science, Springer, Google Scholar, and CNKI, Tables 2 Table 2. MAAs in macroalgal Chlorophytes and Phaeophytes. and 3 are presenteed. In these two tables, all marine macroalgae were grouped according to the typesMAAs of MAAs Greenthat they macroalgae contained. Ref. Brown macroalgae Ref. AS Codium adhaerens, Codium fragile [7] Padina crassa [5] Boodlea compositeTable, Chaetomorpha 2. MAAs in macroalgal Chlorophytes and Phaeophytes. MG tortuosa, Codium adhaerens, Prasiola [4], [7], [34] MAAs Green macroalgae Ref. Brown macroalgae Ref. crispa ssp. antarctica Desmarestia menziesii [5] AS Codium adhaerens, Codium fragile [7] Padina crassa [5] Caulerpa weberiana, Chaetomorpha PE Boodlea composite, Chaetomorpha [7], [34] tortuosa MG tortuosa, Codium adhaerens, Prasiola [4], [7], [34] PL Codium adhaerens [7] Padina crassa [5] crispa ssp. antarctica Desmarestia menziesii [5] Acetabularia mediterranea, Ascophyllum nodosum, Chorda tomentosa, Caulerpa weberiana, Chaetomorpha PE Acrosiphonia arcta, Acrosiphonia [7], [34] Desmarestia aculeata, Desmarestia tortuosa penicilliformis, Caulerpa racemosa, menziesii, Dictyosiphon foeniculaceus, PL Codium adhaerens [2], [7][4], [5], Padina crassa [3–5],[5] [7], PR Cladophora rupestris, Codium Dictyota bartayresii, Halopteris scoparia, [7], [75] [34], [75] Acetabulariaadhaerens, Codium mediterranea fragile,, AscophyllumHimantothallus nodosum grandifolius, Chorda, Hydroclathrus tomentosa, AcrosiphoniaDictyosphaeria arcta, cavernosaAcrosiphonia, clathratusDesmarestia, Padina aculeata crassa,, PilayellaDesmarestia littoralis , penicilliformis, Caulerpa racemosa, menziesii, Dictyosiphon foeniculaceus, Enteromorpha bulbosa, Ulva lactuca [2], [4], [5], Sargassum oligocystum [3–5], [7], PR Cladophora rupestris, Codium Dictyota bartayresii, Halopteris scoparia, Acetabularia mediterranea, Cladophora [7], [75] Desmarestia menziesii, Halopteris scoparia, [34], [75] adhaerens, Codium fragile, Himantothallus grandifolius, Hydroclathrus [3–5], [7], PI rupestris, Codium adhaerens, Codium [7], [75] Himantothallus grandifolius, Padina crassa, Dictyosphaeria cavernosa, clathratus, Padina crassa, Pilayella littoralis, [48] fragile Sargassum oligocystum Enteromorpha bulbosa, Ulva lactuca Sargassum oligocystum Acetabularia mediterranea, Caulerpa Acetabularia mediterranea, Cladophora Desmarestia menziesii, Halopteris scoparia, weberiana, Cladophora rupestris, Ascophyllum nodosum, Desmarestia [3–5],[4], [5],[7], PI rupestris, Codium adhaerens, Codium [2],[7], [5], [75] [7], Himantothallus grandifolius, Padina crassa, SH Codium adhaerens, Codium fragile, aculeata, Fucus spiralis, Halopteris scoparia, [7],[48] [34], fragile [34], [75] Sargassum oligocystum Dictyosphaeria cavernosa, Monostroma Padina crassa, Sargassum oligocystum [75] Acetabulariahariotii, mediterraneaValonia aegagropila, Caulerpa weberiana, Cladophora rupestris, Ascophyllum nodosum, Desmarestia [4], [5], Enteromorpha intestinalis, Prasiola [2], [5], [7], SHUN Codium adhaerens, Codium fragile, [2], [75] aculeata, Fucus Prasiolaspiralis, crispaHalopteris scoparia, [7],[49] [34], stipata, Prasiola crispa ssp. antarctica [34], [75] Dictyosphaeria cavernosa, Monostroma Padina crassa, Sargassum oligocystum [75] Note: AS, Asterina-330; MG, Mycosporine-glycine; PE, Palythene; PL, Palythinol; PR, Porphyra-334; hariotii, Valonia aegagropila PI, Palythine; SH, Shinorine; UN, Unidentified MAAs. Enteromorpha intestinalis, Prasiola UN [2], [75] Prasiola crispa [49] stipata, Prasiola crispa ssp. antarctica Table 3. MAAs in macroalgal Rhodophytes. Note: AS, Asterina-330; MG, Mycosporine-glycine; PE, Palythene; PL, Palythinol; PR, Porphyra-334; MAAsPI, Palythine; Red macroalgae SH, Shinorin e; UN, Unidentified MAAs. Ref. APA Agarophyton chilense, Bostrychina arbusculaa, Ceramium sp.a, Euptilota formosissimaa, Gigartina [71] Table 3. MAAs in macroalgal Rhodophytes.

MAAs Red macroalgae Ref. APA Agarophyton chilense, Bostrychina arbusculaa, Ceramium sp.a, Euptilota formosissimaa, Gigartina [71]

Mar. Drugs 2020, 18, 43 10 of 23

Table 2. MAAs in macroalgal Chlorophytes and Phaeophytes.

MAAs Green Macroalgae Ref. Brown Macroalgae Ref. AS Codium adhaerens, Codium fragile [7] Padina crassa [5] Boodlea composite, Chaetomorpha MG tortuosa, Codium adhaerens, [4,7,34] Desmarestia menziesii [5] Prasiola crispa ssp. antarctica Caulerpa weberiana, PE [7,34] Chaetomorpha tortuosa PL Codium adhaerens [7] Padina crassa [5] Ascophyllum nodosum, Chorda Acetabularia mediterranea, Acrosiphonia tomentosa, Desmarestia aculeata, arcta, Acrosiphonia penicilliformis, Desmarestia menziesii, Dictyosiphon Caulerpa racemosa, Cladophora rupestris, foeniculaceus, Dictyota bartayresii, PR [2,4,5,7,75] [3–5,7,34,75] Codium adhaerens, Codium fragile, Halopteris scoparia, Himantothallus Dictyosphaeria cavernosa, Enteromorpha grandifolius, Hydroclathrus clathratus, bulbosa, Ulva lactuca Padina crassa, Pilayella littoralis, Sargassum oligocystum Acetabularia mediterranea, Cladophora Desmarestia menziesii, Halopteris PI rupestris, Codium adhaerens, [7,75] scoparia, Himantothallus grandifolius, [3–5,7,48] Codium fragile Padina crassa, Sargassum oligocystum Acetabularia mediterranea, Caulerpa Ascophyllum nodosum, Desmarestia weberiana, Cladophora rupestris, Codium aculeata, Fucus spiralis, Halopteris SH adhaerens, Codium fragile, [2,5,7,34,75] [4,5,7,34,75] scoparia, Padina crassa, Dictyosphaeria cavernosa, Monostroma Sargassum oligocystum hariotii, Valonia aegagropila Enteromorpha intestinalis, Prasiola UN [2,75] Prasiola crispa [49] stipata, Prasiola crispa ssp. antarctica Note: AS, Asterina-330; MG, Mycosporine-glycine; PE, Palythene; PL, Palythinol; PR, Porphyra-334; PI, Palythine; SH, Shinorine; UN, Unidentiﬁed MAAs.

Table 3. MAAs in macroalgal Rhodophytes.

MAAs Red Macroalgae Ref. Agarophyton chilense, Bostrychina arbuscula a, Ceramium sp. a, Euptilota formosissima a, Gigartina macrocarpa a, APA Hymenena affinis, Mastocarpus stellatus a, Porphyra umbilicalis a, Pyropia columbina a, Pyropia plicata a, [71] Rhodophyllis membranecea a, Sarcothalia atropurpurea a, Spongoclonium pastorale a Agarophyton chilense, Champia novae-zelandiae, Gigartina macrocarpa, Porphyra umbilicalis, Pyropia columbina, APB [71] Pyropia plicata, Sarcothalia atropurpurea Acanthophora muscoides, Acanthophora specifera, Agarophyton chilense, Amansia multifida, Ahnfeltiopsis devoniensis, Actinotrichia fragilis, Arthrocardia gardneri, Asparagopsis armata, Bangia atropurpurea, Bonnemaisonia hamifera, Bostrychia arbuscula, Bostrychia calliptera, Bostrychia montagnei, Bostrychia moritziana, Bostrychia radicans, Bostrychia scorpioides, Bostrychia simpliciuscula, Bryothamnion seaforthii, Bostrychia tenella, Bryothamnion triquetrum, Caloglossa apomeiotica, Caloglossa leprieurii, Calliarthron tuberculosum, Caloglossa stipitata, Caloglossa ogasawaraensis, Centroceras clavulatum, Ceramium nodulosum, Ceramium sp., Ceramium secundatum, Champia novae-zelandiae, Chondracanthus acicularis, Chondracanthus elegans, Chondracanthus teedei, Chondrus crispus, Chondrus ocellatus, Corallina officianalis var. chilensisa, Corallina officinalis, Corallina sp., Corallina vancouveriensis, Craspedocarpus erosus, Cryptonemia crenulata, Curdiea racovitzae, Devaleraea ramentacea, Dichotomaria marginata, Digenea simplex, Ellisolandia elongata, Euptilota formosissima, Gastroclonium ovatum, Gelidiella acerosa, Gelidiopsis variabilis, Gelidium amansii, Gelidium crinale, Gelidium corneum, Gelidium floridanum, Gelidium pusillum, Gelidium sesquipedale, Gloiopeltis furcata, Gigartina macrocarpa, Gigartina pistillata, Gigartina skottsbergii, Gracilaria caudata, Gracilaria changii, Gracilaria chilensis, [3–7,32,35,37,39–42,44, AS Gracilaria cornea, Gracilaria conferta, Gracilaria eucheumoides, Gracilaria domingensis, Gracilaria saliconia, 48,49,51,52,55,66,67,70, Gracilaria tenuistipitata, Gracilaria vermiculophylla, Gracilariopsis longissima, Gracilariopsis tenuifrons, 71,74,75,78–81,95–104] Gymnogongrus antarctica, Gymnogongrus antarcticus, Gymnogongrus griffithsiae, Hypnea musciformis, Hypnea spinella, Iridaea chordata, Jania adhaerens, Jania crassa, Jania cubensis, Jania rubens, Jania subulata, Kallymenia antarctica, Laurencia caraibica, Laurencia cartilaginea, Laurencia changii, Laurencia dendroidea, Laurencia filiformis, Laurencia obtusa, Lithophyllum incrustans, Lithophyllum expansum, Mastocarpus stellatus, Mazzaella flaccida, Mazzaella laminarioides, Myriogramme manginii, Notophycus fimbriatus, Osmundea hybrid, Osmundea pinnatitida, Osmundea spectabilis, Pachymenia laciniata, Palmaria decipiens, Palmaria palmata, Palisada flagellifera, Palisada perforate, Phyllophora appendiculata, Plocamium cartilagineum, Polysiphonia arctica, Porphyra endiviifolium, Porphyra columbina, Porphyra leucosticta, Porphyra rosengurttii, Porphyra ssp., Prionitis lanceolata, Pterocladiella capillacea, Pyropia acanthophora, Pyropia columbina, Pyropia plicata, Rhodophyllis membranecea, Rhodymenia pseudopalmata, Sarcothalia atropurpurea, Solieria filiformis, Spongoclonium pastorale, Spyridia clavata, Stictosiphonia arbuscula, Stictosiphonia hookeri, Stictosiphonia intricate, Stictosiphonia tangatensis, Tricleocarpa cylindrica, Vertebrata lanosa Mar. Drugs 2020, 18, 43 11 of 23

Table 3. Cont.

MAAs Red Macroalgae Ref. CL Catenella caespitosa, Catenella repens, Catenella nipae [49,72] Champia novae-zelandiae, Ceramium sp., Gigartina macrocarpa, Mastocarpus stellatus, Porphyra umbilicalis, MAG Pyropia columbina, Pyropia plicata, Rhodophyllis membranecea, Sarcothalia atropurpurea, [78] Spongoclonium pastorale Acanthophora muscoides, Acanthophora specifera, Agarophyton chilense, Apophlaea lyallii, Blastophyllis calliblepharoides, Bostrychia moritziana, Bostrychia radicans, Bostrychia scorpioides, Centroceras clavulatum, Ceramium rubrum, Ceramium sp., Champia novae-zelandiae, Chondria arinata, Curdiea racovitzae, Devaleraea ramentacea, Dumontia incrassata a, Gracilaria caudata, Gracilaria cornea, Grateloupia lanceola, Gymnogongrus [2–7,32,34,35,37,40,42– MG turquetii, Hypnea spinella, Iridaea chordata, Jania subulata, Kallymenia antarctica, Laurencia caraibica, Laminaria 45,55,69,71,74–78] saccharina, Mazzaella laminarioides, Notophycus fimbriatus, Osmundaria obtusiloba, Pachymenia orbicularis, Palmaria decipiens, Palmaria palmata, Phyllophora antarctica, Phyllophora appendiculata, Porphyra columbina, Porphyra endiviifolium, Porphyra purpurea-violacea, Pyropia plicata, Rhodymenia spp., Sarcothalia atropurpurea, Schizymenia apoda, Spongoclonium pastorale Agarophyton chilense, Ceramium sp., Porphyra umbilicalis, Pyropia columbina, Pyropia plicata, MMT [77] Sarcothalia atropurpurea M2G Gloiopeltis furcata [40] Acanthophora specifera, Actinotrichia fragilis, Agarophyton chilense, Bangia atropurpurea, Bostrychia simpliciuscula, Ceramium nodulosum, Chondrus crispus, Curdiea racovitzae, Devaleraea ramentacea, Gigartina macrocarpa, Gracilaria changii, Gracilaria chilensis, Gracilaria tenuistipitata, Gracilariopsis tenuifrons, Gracilaria [3–5,32,34,40–44,70,75, PE vermiculophylla, Iridaea chordata, Osmundea hybrid, Osmundea pinnatitida, Palmaria decipiens, Palmaria palmata, 77,96,99,102,104] Phyllophora antarctica, Phyllophora appendiculata, Porphyra purpurea-violacea, Pyropia plicata, Rhodymenia pseudopalmata, Sarcothalia atropurpurea, Spongoclonium pastorale, Stictosiphonia hookeri, Vertebrata lanosa PA Solieria chordalis [54] Acanthophora specifera, Actinotrichia fragilis, Bangia atropurpurea, Bostrychia calliptera, Bostrychia montagnei, Bostrychia moritziana, Bostrychia radicans, Bostrychia simpliciuscula, Bostrychia tenella, Caloglossa leprieurii, Chondria arinata, Chondrus crispus, Corallina vancouveriensis, Curdiea racovitzae, Devaleraea ramentacea, Ellisolandia elongata, Gelidium corneum, Gelidium pusillum, Gelidium sesquipedale, Gracilaria changii, Gracilaria [3–5,32,35,37,39–42,44, chilensis, Gracilaria cornea, Gracilaria domingensis, Gracilaria eucheumoides, Gracilaria saliconia, Gracilaria PL 45,48,52,55,65,67,75,79, tenuistipitata, Gracilariopsis longissima, Gracilariopsis tenuifrons, Halopythis incurve, Iridaea chordata, 96–99,102,104,105] Kallymenia antarctica, Laurencia cartilaginea, Laurencia changii, Laurencia obtusa, Mazzaella flaccida, Mastocarpus stellatus, Osmundea spectabilis, Palmaria decipiens, Palmaria palmata, Plocamium cartilagineum, Polysiphonia arctica, Porphyra endiviifolium, Rhodymenia pseudopalmata, Rhodymenia spp., Stictosiphonia intricate, Stictosiphonia tangatensis Acanthophora muscoides, Acanthophora specifera, Actinotrichia fragilis, Agarophyton chilense, Amansia multifida, Arthrocardia gardneri, Asparagopsis armata, Asparagopsis taxiformis, Bangia atropurpurea, Bangia fuscopurpurea, Blastophyllis calliblepharoides, Bostrychia arbuscula, Bostrychia calliptera, Bostrychia harveyi, Bostrychia montagnei, Bostrychia moritziana, Bostrychia radicans, Bostrychia scorpioides, Bostrychia simpliciuscula, Bostrychia tenella, Bryothamnion seaforthii, Calliarthron tuberculosum, Caloglossa apomeiotica, Caloglossa leprieurii, Caloglossa ogasawaraensis, Caloglossa stipitata, Calliarthron tuberculosum, Catenella nipae, Ceramium nodulosum, Ceramium sp., Champia novae-zelandiae, Chondracanthus acicularis, Chondria arinata, Chondrus crispus, Corallina officinalis, Corallina officianalis var. chilensisa, Corallina vancouveriensis, Craspedocarpus erosus, Curdiea racovitzae, Cystoclonium purpureum, Devaleraea ramentacea, Dumontia incrassata, Endocladia muricata, Euptilota formosissima, Galaxaura oblongata, Ganonema farinosa, Gastroclonium ovatum, Gelidiella acerosa, Gelidiopsis variabilis, Gelidium amansii, Gelidium crinale, Gelidium corneum, Gelidium floridanum, Gelidium pusillum, Gelidium sesquipedale, Georgiella confluens, Gigartina macrocarpa, Gigartina skottsbergii, Gloiopeltis furcata, Gracilaria birdiae, Gracilaria caudata, Gracilaria changii, Gracilaria chilensis, Gracilaria conferta, Gracilaria cornea, Gracilaria domingensis, Gracilaria eucheumoides, Gracilaria saliconia, Gracilaria [1,3–7,32,34,35,37,40– vermiculophylla, Gracilaria tenuistipitata, Grateloupia lanceola, Gymnogongrus griffithsiae, Halopythis incurve, 42,44,45,47,48,51,52,55, PR Hymenena affinis, Hydropuntia cornea, Hypnea musciformis, Hypnea spinella, Iridaea sp., Iridaea chordata, Jania 57,58,65–67,69,71,74– adhaerens, Jania rubens, Kallymenia antarctica, Laurencia caraibica, Laurencia cartilaginea, Laurencia changii, 79,84–88,90–92,95,100, Laurencia dendroidea, Laurencia filiformis, Laurencia obtusa, Lithophyllum expansum, Lithophyllum incrustans, 102,104–107] Lithothamnion antarcticum, Lithophyllum expansum, Mazzaella flaccida, Mastocarpus jardinii, Mastocarpus papillatus, Mastocarpus stellatus, Myriogramme manginii, Neuroglossum ligulatum, Nodularia spumigena, Notophycus fimbriatus, Osmundea hybrid, Osmundaria obtusiloba, Osmundea spectabilis, Pachymenia laciniata, Pachymenia orbicularis, Palmaria decipiens, Palmaria palmata, Palisada flagellifera, Palisada perforate, Pantoneura plocamioides, Plocamium cartilagineum, Phyllophora antarctica, Polysiphonia arctica, Porphyra dioica, Porphyra endiviifolium, Porphyra leucosticta, Porphyra plocamiestris, Porphyra purpurea, Porphyra purpurea-violacea, Porphyra rosengurttii, Porphyra sp., Porphyra tenera, Porphyra umbilicalis, Porphyra yezoensis, Porphyra vietnamensis, Prionitis lanceolata, Pseudolithophyllum expansum, Pterocladiella capillacea, Pterocladia sp., Ptilota plumosa, Pyropia acanthophora, Pyropia columbina, Pyropia plicata, Rhodophyllis membranecea, Rhodymenia pseudopalmata, Rhodymenia spp., Rhodymenia subantarctica, Sarcothalia atropurpurea, Schizymenia apoda, Scinaia boergesenii, Spongoclonium pastorale, Spyridia clavata, Spyridia filamentosa, Stictosiphonia arbuscula, Stictosiphonia hookeri, Stictosiphonia intricate, Stictosiphonia tangatensis, Tricleocarpa cylindrical, Vertebrata lanosa Mar. Drugs 2020, 18, 43 12 of 23

Table 3. Cont.

MAAs Red Macroalgae Ref. Acanthophora muscoides, Acanthophora specifera, Agarophyton chilense, Amansia multifida, Amphiroa rigida, Ahnfeltiopsis devoniensis, Arthrocardia gardneri, Asparagopsis armata, Asparagopsis taxiformis, Bangia atropurpurea, Blastophyllis calliblepharoides, Bonnemaisonia hamifera, Bostrychia arbuscula, Bostrychia calliptera, Bostrychia harveyi, Bostrychia moritziana, Bostrychia montagnei, Bostrychia pinnata, Bostrychia radicans, Bostrychia scorpioides, Bryothamnion seaforthii, Bostrychia tenella, Bryothamnion triquetrum, Calliarthron tuberculosum, Caloglossa ogasawaraensis, Centroceras clavulatum, Ceramium nodulosum, Ceramium secundatum, Ceramium sp., Champia novae-zelandiae, Chondracanthus acicularis, Chondracanthus chamissoi, Chondracanthus elegans, Chondracanthus teedei, Chondria arinata, Chondrus crispus, Chondrus ocellatus, Chondrus yendoi, Corallina elongata, Corallina officinalis, Corallina officianalis var. chilensisa, Corallina sp., Corallina vancouveriensis, Craspedocarpus erosus, Cryptonemia crenulata, Curdiea racovitzae, Devaleraea ramentacea, Dichotomaria marginata, Digenea simplex, Dumontia incrassata a, Ellisolandia elongata, Endocladia muricata, Euptilota formosissima, Gastroclonium ovatum, Gelidiella acerosa, Gelidiopsis variabilis, Gelidium amansii, Gelidium corneum, Gelidium crinale, Gelidium floridanum, Gelidium lingulatum, Gelidium pusillum, Gelidium sesquipedale, Georgiella confluens, Gigartina macrocarpa, Gigartina pistillata, Gigartina skottsbergii, Gracilaria asiatica, Gracilaria birdiae, Gracilaria caudata, Gracilaria changii, Gracilaria chilensis, Gracilaria conferta, [3–7,32,34–37,39–46,48, Gracilaria cornea, Gracilaria domingensis, Gracilaria eucheumoides, Gracilaria saliconia, Gracilaria tenuistipitata, 50,52,55,56,58,65–71, PI Gracilaria vermiculophylla, Gracilariopsis longissima, Grateloupia lanceola, Gymnogongrus Antarctica, 75–79,82–84,90,91,95, Gymnogongrus antarcticus, Gymnogongrus griffithsiae, Halopythis incurve, Hymenena affinis, Hypnea 97,100–102,108–110] musciformis, Hypnea spinella, Hypoglossum hypoglossoides, Iridaea chordata, Iridaea sp., Jania adhaerens, Jania crassa, Jania cubensis, Jania rubens, Jania subulata, Kallymenia antarctica, Laurencia caraibica, Laurencia cartilaginea, Laurencia changii, Laurencia dendroidea, Laurencia filiformis, Laurencia obtusa, Lithophyllum incrustans, Lithophyllum expansum, Lithothamnion antarcticum, Lomentaria articulate, Mastocarpus jardinii, Mastocarpus stellatus, Mazzaella flaccida, Mazzaella laminarioides, Myriogramme manginii, Neuroglossum ligulatum, Notophycus fimbriatus, Osmundea hybrid, Osmundaria obtusiloba, Osmundea pinnatitida, Osmundea spectabilis, Pachymenia laciniata, Pachymenia orbicularis, Palmaria decipiens, Palmaria palmata, Palisada flagellifera, Palisada perforate, Phyllophora antarctica, Phyllophora appendiculata, Plocamium cartilagineum, Polysiphonia arctica, Polysiphonia urceolata, Porphyra leucosticta, Porphyra purpurea-violacea, Porphyra rosengurttii, Porphyra sp., Porphyra yezoensis, Porphyra umbilicalis, Prionitis lanceolata, Pterocladiella capillacea, Pterocladia sp., Pyropia columbina, Pyropia acanthophora, Pyropia plicata, Rhodophyllis membranecea, Rhodymenia pseudopalmata, Rhodymenia spp., Sarcothalia atropurpurea, Sarcothalia papillosa, Schizymenia apoda, Scinaia boergesenii, Solieria filiformis, Solieria pacifica, Spongoclonium pastorale, Stictosiphonia arbuscula, Stictosiphonia intricate, Stictosiphonia tangatensis, Tricleocarpa cylindrical, Vertebrata lanosa Acanthophora muscoides, Acanthophora spicifera, Actinotrichia fragilis, Agarophyton chilense, Ahnfeltiopsis devoniensis, Amansia multifida, Amphiroa rigida, Amphiroa sp., Ahnfeltiopsis devoniensis, Arthrocardia gardneri, Asparagopsis armata, Asparagopsis taxiformis, Bangia atropurpurea, Bangia fuscopurpurea, Bangia sp., Bonnemaisonia hamifera, Bostrychina arbuscula, Bostrychia calliptera, Bostrychia moritziana, Bostrychia montagnei, Bostrychia moritziana, Bostrychia scorpioides, Bostrychia simpliciuscula, Bostrychia tenella, Bryothamnion seaforthii, Bryothamnion triquetrum, Callithamnion tetragonum, Caloglossa apomeiotica, Caloglossa leprieurii, Caloglossa ogasawaraensis, Caloglossa stipitata, Calliarthron tuberculosum, Centroceras clavulatum, Ceramium echionotum, Ceramium nodulosum, Ceramium rubrum, Ceramium secundatum, Ceramium sp., Champia novae-zelandiae, Chondracanthus acicularis, Chondracanthus chamissoi, Chondracanthus elegans, Chondracanthus teedei, Chondria arinata, Chondrus crispus, Chondrus yendoi, Corallina elongata, Corallina officinalis, Corallina officianalis var. chilensisa, Corallina sp., Corallina vancouveriensis, Craspedocarpus erosus, Cryptonemia crenulata, Curdiea racovitzae, Cystoclonium purpureum a, Devaleraea ramentacea, Dichotomaria marginata, Digenea simplex, Dumontia incrassata a, Ellisolandia elongata, Endocladia muricata, Euptilota formosissima, Galaxaura oblongata, Ganonema farinosa, Gastroclonium ovatum, Gelidiella acerosa, Gelidiopsis variabilis, Gelidium amansii, Gelidium corneum, Gelidium crinale, Gelidium floridanum, Gelidium latifolium, Gelidium lingulatum, Gelidium pusillum, Gelidium sp., Gelidium sesquipedale, Georgiella confluens, Gloiopeltis furcata, Gigartina macrocarpa, Gigartina pistillata, Gigartina skottsbergii, Gracilaria birdiae, Gracilaria [1,3–7,32,34–40,42–45, caudata, Gracilaria cornea, Gracilaria changii, Gracilaria chilensis, Gracilaria conferta, Gracilaria cornea, 48,50–53,55–57,66–68, SH Gracilaria domingensis, Gracilaria eucheumoides, Gracilaria gracilis, Gracilaria saliconia, Gracilaria tenuistipitata, 70,71,75–79,82,84–86, Gracilaria vermiculophylla, Gracilariopsis longissima, Grateloupia doryphora, Gymnogongrus Antarctica, 90–92,96,98,101,103, Gymnogongrus antarcticus, Gymnogongrus griffithsiae, Gymnogongrus turquetii, Halopythis incurve, Hypnea 105,108,110–113] musciformis, Hypnea spinella, Hypoglossum hypoglossoides, Iridaea chordata, Iridaea sp., Jania adhaerens, Jania crassa, Jania cubensis, Jania rubens, Jania subulata, Kallymenia antarctica, Laurencia caraibica, Laurencia changii, Laurencia dendroidea, Laurencia filiformis, Laurencia obtusa, Lithophyllum expansum, Lithophyllum incrustans, Lithophyllum expansum, Lithothamnion antarcticum, Lomentaria articulate, Mazzaella flaccida, Mazzaella laminarioides, Mastocarpus jardinii, Mastocarpus papillatus, Mastocarpus stellatus, Myriogramme manginii, Neuroglossum ligulatum, Notophycus fimbriatus, Osmundaria obtusiloba, Osmundea pinnatitida, Osmundea spectabilis, Pachymenia laciniata, Palmaria decipiens, Palmaria palmata, Palisada flagellifera, Palisada perforate, Pantoneura plocamioides, Phyllophora antarctica, Phyllophora appendiculata, Plocamium cartilagineum, Polysiphonia arctica, Porphyra dioica, Porphyra endiviifolium, Polysiphonia urceolata, Porphyra haitanensis, Porphyra leucosticta, Porphyra plocamiestris, Porphyra purpurea, Porphyra rosengurttii, Porphyra sp., Porphyra umbilicalis, Porphyra yezoensis, Prionitis lanceolata, Pseudolithophyllum expansum a, Pterocladia lucida, Pterocladiella capillacea, Pterocladia sp., Pyropia acanthophora, Pyropia columbina, Pyropia plicata, Rhodomela virgata, Rhodophyllis membranecea, Rhodymenia pseudopalmata, Rhodymenia spp., Rissoella verruculosa, Sarcothalia atropurpurea, Sarcothalia papillosa, Schizymenia apoda, Scinaia boergesenii, Spongoclonium pastorale, Spyridia clavata, Stictosiphonia arbuscula, Stictosiphonia hookeri, Stictosiphonia intricate, Stictosiphonia tangatensis, Trichocarpus crinitus, Tricleocarpa cylindrica Mar. Drugs 2020, 18, 43 13 of 23

Table 3. Cont.

MAAs Red Macroalgae Ref. Agarophyton chilense, Bostrychia scorpioides, Calliarthron tuberculosum, Ceramium nodulosum, Ceramium sp., Chondracanthus acicularis, Corallina officianalis var. chilensisa, Corallina vancouveriensis, Gigartina macrocarpa, Gracilariopsis tenuifrons, Gracilaria vermiculophylla, Mastocarpus papillatus, Mastocarpus stellatus, Mazzaella [4,6,37,39,52,55,70,76– US flaccida, Osmundea hybrid, Osmundea pinnatitida, Palmaria decipiens, Palmaria palmata, Phyllophora Antarctica, 78,104] Prionitis lanceolata, Pterocladiella capillacea, Pyropia plicata, Rhodophyllis membranecea, Rhodymenia pseudopalmata, Sarcothalia atropurpurea, Spongoclonium pastorale, Vertebrata lanosa NM Bostrychia scorpioides, Gracilaria vermiculophylla [70,71] Ahnfeltiopsis devoniensis I~II, Asparagopsis armata, Bonnemaisonia hamifera, Bostrychia calliptera, Bostrychia scorpioides I~II, Bostrychia sp., Callithamnion tetragonum, Callophyllis variegata, Catenella caespitosa I~II, Catenella nipae I~IX, Catenella impudica, Catenella repens I~II, Ceramium nodulosum I~II, Ceraminum rubrum, Ceramium secundatum I~II, Chondracanthus acicularis I~II, Chondria arinata, Chondrus crispus I~II, Chondrus ocellatus, Corallina officinalis, Corallina sp. I~II, Curdiea racovitzae I~II, Devaleraea ramentacea, Gastroclonium ovatum, Gelidium corneum I~II, Gigartina pistillata I~II, Gigartina skottsbergii, Gigartina skottsbergii, Gracilaria changii, Gracilaria conferta, Gracilaria gracilis, Gracilaria lemaneiformis I~II, Gracilaria vermiculophylla I~III, [1,3,4,6,7,37,40,44,47, UN Gracilariopsis longissima, Gracilariopsis tenuifrons, Hypoglossum hypoglossoides, Iridaea chordata, Iridaea 54,57,69,70,75,86,88,90, tuberculosa, Jridaea cordata, Kallymenia antarctica, Lophurella hoockeriana, Mazzaella laminarioides, Mastocarpus 102,105,114,115] stellatus I~II, Myriogramme manginii, Neuroglossum ligulatum, Nothogenia fastigiata, Notophycus fimbriatus, Nothogenia sp., Osmundea hybrid, Osmundea pinnatitida, Palmaria decipiens, Palmaria palmata I~III, Phyllophora truncata, Polysiphonia arctica, Polysiphonia sp., Porphyra dioica, Porphyra endiviifolium, Porphyra rosengurttii, Porphyria spec., Porphyra yezoensis, Pseudolithophyllum expansum, Ptilota gunneri, Ptilonia magellanica, Pyropia columbina, Rhodomela confervoides, Sarcothalia crispata, Sarcothalia papillosa, Schizoseris sp., Solieria chordalis, Vertebrata lanosa Note: APA, Aplysiapalythine A [a. Tentative identification]; APB, Aplysiapalythine B; AS, Asterina-330; CL, Catenelline; MAG, mycosporine-alanine-glycine; MG, Mycosporine-glycine; MMT, mycosporine-methylamine- threonine; M2G, Mycosporine-2-glycine; PE, Palythene; PA, Palythenic acid; PI, Palythine; PL, Palythinol; PR, Porphyra-334; PS, Palythine-serine; SH, Shinorine; SME, Shinorine methyl ester; US, Usujirene; NM, Novel MAAs; UN, Unidentified MAAs.

2.2. An Open Database for MAAs in Marine Macroalgae In order for the scientists in the field to have a more comprehensive and clearer understanding of MAAs in marine macroalgae, it was necessary to establish a corresponding database. Therefore, our project team established a database (http://210.28.32.218/MAAs/) of MAAs in marine macroalgae over the past nearly 30 years utilizing data information from the Web of Science, Springer, Google Scholar and CNKI. In this database, more detailed information in relation to algal MAAs, such as the total contents of MAAs, content of specific MAA, type of MAAs, origin of marine macroalgae, and/or composition of specific MAA in MAAs, was listed. This was the comprehensive summary database of MAAs in marine macroalgae at home and abroad, and it was open and free. Up to now, it has been determined that 572 species of marine macroalgae contained MAAs. Among them, MAAs contents and/or MAAs composition in 501 species have been reported. Therefore, related informations of MAAs in 501 species of marine macroalgae since 1990 have been getted using our database for MAAs in marine macroalgae. In the following work process, we will try to expand the sources of the reports collection and its published time in order to provide more complete data about MAAs in marine macroalgae.

2.3. Marine Macroalgae with No Detectable MAAs Concentrations MAAs accumulation in marine macroalgae were widespread and but not ubiquitous characteristics, and some marine macroalgae did not contain MAAs with detectable concentrations. We found that these marine macroalgae distributed in 18 orders (Figure6) and its numbers were more than 100 species (Table4) in the past 30 years. From Figure6 it appeared that marine macroalgae with no detectable MAA concentrations have a wide taxonomic distribution. Mar. Drugs 2020, 18 FOR PEER REVIEW 15

The green algae (21 species) in Chlorophyta, the brown algae (37 species) in Phaeophyta, and the red algae (45 species) in Rhodophyta were confirmed to have no detectable MAAs concentrations (Table 4), such as macroalgal Chlorophytes Acrosiphonia arcta [3], Acrosiphonia penicilliformis [3], Anadyomene wrightii [3], and etc. [3]; macroalgal Phaeophytes Adenocystis utricularis Mar.[3], Drugs Alaria2020 esculenta, 18, 43 [3], Ascoseira mirabilis [3], and others brown algae [3]; macroalgal Rhodophytes14 of 23 Antarcticothamnion polysporum [3], Heterosiphonia plumosa [70], Odonthalia dentate [4], and so on [3,70].

111 Acrochaetiales Ascoseirales 9 1 2 2 21 Balliales Bangiales 6

Ceramiales Chordales

Cladophrales Corallinales 11 2 Desmarestiales Dictyotales

Ectocarpales Fucales 10

Gigartinales Laminariales 12 2 Rhodymeniales Tilopteridales 3 8 5 6 Ulotrichales Ulvales

Figure 6. Distribution of marine macroalgae with no detectable MAAs concentrations. Data collected fromFigure related 6. Distribution studies since of marine 1990, andmacroalgae the number with no in adetectable pie chart MAAs represents concentrations. the number Data of collected marine macroalgaefrom related belonging studies tosince these 1990, orders. and the number in a pie chart represents the number of marine macroalgae belongingTable 4. Marineto these macroalgaeorders. with no detectable MAAs concentrations.

Table 4. Marine macroalgae withMarine no detectable Macroalgae MAAs concentrations. Acrosiphonia arcta [3], Acrosiphonia penicilliformis [3], Anadyomene wrightii [3], Boergesenia forbesii [3], Chaetomorpha linum [3], Chaetomorpha melagoniumMarine Macroalgae[3], Cladophora rupestris [3], Enteromorpha Chlorophyta Acrosiphoniacompressa [ 3arcta], Enteromorpha [3], Acrosiphonia intestinalis penicilliformis[3], Enteromorpha [3], Anadyomenesp. [3], wrightiiEnteromorpha [3], Boergeseniaspp. [3], Monostromaforbesii [3], nitidum [3], Monostoma arcticum [3], Ulva conglohata [3], Ulva fasciata [3], Ulva lactuca [3], Ulva Chaetomorphaolivascens [3 ],linumUlva [3], rotundata Chaetomorpha[3], Valoniopsis melagonium pachynema [3], Cladophora[3] rupestris [3], Enteromorpha compressa [3], Chlorophyta EnteromorphaAdenocystis utricularisintestinalis[ 3[3],], Alaria Enteromorpha esculenta sp.[3 ],[3],Ascoseira Enteromorpha mirabilis spp.[3], [3],Chnoospora Monostroma implexa nitidum[3], [3],Chorda Monostomafilum [3], Chordaria arcticum [3], flagelliformis Ulva conglohata[3], Colpomenia [3], Ulva fasciata sinuosa [3],[3], UlvaCystoseira lactuca usneoides [3], Ulva[ 3olivascens], Desmarestia [3], Ulva aculeata [3], Desmarestia menziesii [3], Dictyota dichotoma [3], Fucus distichus [3], Fucus serratus [3], Fucus rotundata [3], Valoniopsis pachynema [3] Phaeophyta spiralis [3], Fucus vesiculosus [3], Kjellmaniella crassifolia [3], Laminaria digitata [3], Laminaria Adenocystishyperborean utricularis[3], Laminaria [3], Alaria japonica esculenta[3], Laminaria [3], Ascoseira ochroleuca mirabilis[3], [3],Laminaria Chnoospora saccharina implexa[3 ],[3],Laminaria Chorda filum solidungula [3], Padina boryana [3], Padina pavonica [3], Phaeurus antarcticus [3], Saccorhiza dermatodea [3], [3], Chordaria flagelliformis [3], Colpomenia sinuosa [3], Cystoseira usneoides [3], Desmarestia aculeata [3], Saccorhiza polyschides [3], Sargassum muticum [3] Desmarestia menziesii [3], Dictyota dichotoma [3], Fucus distichus [3], Fucus serratus [3], Fucus spiralis [3], Antarcticothamnion polysporum [3], Audouinella purpurea [3], Ballia callitricha [3], Bornetia secundiflora [70], Phaeophyta FucusCalliblepharis vesiculosus jubata [3], [Kjellmaniella70], Callithamnion crassifolia tetragonum [3], Laminaria[70], Champia digitata parvula[3], Laminaria[70], Chylocladia hyperborean verticillata [3], Laminaria[70], japonicaDelesseria [3],lancifolia Laminaria[3 ],ochroleucaDelesseria [3], sanguinea Laminaria[3], saccharinaDilsea carnosa [3], Laminaria[76], Furcellaria solidungula lumbricalis [3], Padina[3,76], boryanaGriffithsia [3], corallinoides [70], Hymenocladiopsis crustigena [3], Heterosiphonia plumosa [70], Membranoptera alata [70], Rhodophyta PadinaMetacallophyllis pavonica [3], laciniata Phaeurus[70 ],antarcticusMyriogramme [3], Saccorhiza smithii [3], dermatodeaOdonthalia [3], dentate Saccorhiza[4], Pantoneura polyschides plocamioides [3], Sargassum[3], muticumPhyllophora [3] ahnfeltioides [3], Phycodrys austrogeorgica [3], Phycodrys rubens [3,71], Phycodrys quercifolia [3], Phyllophora truncata [3], Picconiella plumosa [3], Plocamium cartilagineum [3], Plumaria plumosa [70], Antarcticothamnion polysporum [3], Audouinella purpurea [3], Ballia callitricha [3], Bornetia secundiflora [70], Porphyra plocamiestris [3], Ptilota serrate [3], Polysiphonia elongata [3], Polyides rotundus [3], CalliblepharisSphaerococcus jubata coronopifolius [70], Callithamnion[70] tetragonum [70], Champia parvula [70], Chylocladia verticillata [70], Delesseria lancifolia [3], Delesseria sanguinea [3], Dilsea carnosa [76], Furcellaria lumbricalis [3,76], Griffithsia The green algaecorallinoides (21 species) [70], Hymenocladiopsis in Chlorophyta, crustigena the brown [3], Heterosiphonia algae (37 species)plumosa [70], in Phaeophyta,Membranoptera alata and [70], the red algaeRhodophyta (45 species) Metacallophyllis in Rhodophyta laciniata were [70], confirmed Myriogramme to smithii have [3], no Odonthalia detectable dentate MAAs [4], Pantoneura concentrations plocamioides (Table [3],4 ), such as macroalgalPhyllophora Chlorophytes ahnfeltioidesAcrosiphonia [3], Phycodrys austrogeorgica arcta [3], Acrosiphonia [3], Phycodrys rubens penicilliformis [3,71], Phycodrys[3], quercifoliaAnadyomene [3], wrightii [3], and etc.Phyllophora [3]; macroalgal truncata [3], Phaeophytes Picconiella plumosaAdenocystis [3], Plocamium utricularis cartilagineum[3], [3],Alaria Plumaria esculenta plumosa[3 [70],], Ascoseira mirabilis [3], andPorphyra others plocamiestris brown algae [3], Ptilota [3]; macroalgal serrate [3], Polysiphonia Rhodophytes elongataAntarcticothamnion [3], Polyides rotundus [3], polysporum Sphaerococcus[ 3], Heterosiphonia plumosacoronopifolius[70], [70]Odonthalia dentate [4], and so on [3,70]. MAAs were an important class of bioactive secondary metabolites in marine macroalgae [67,68], their types and accumulation were variable with some environmental variables, including radiation [6,74,77,81,116], nutrients [6,74,77,81], salinity [44], temperature [116], and desiccation [113,117]. These studies were not included in this paper. Mar. Drugs 2020, 18 FOR PEER REVIEW 16

MAAs were an important class of bioactive secondary metabolites in marine macroalgae [67,68], their types and accumulation were variable with some environmental variables, including radiation [6,74,77,82,117], nutrients [6,74,77,82], salinity [44], temperature [117], and desiccation [114,118]. These studies were not included in this paper.

2.4. Trends in Research on MAAs in Marine Macroalgae Figure 7 shows a cluster view of studies about MAAs in marine macroalgae in the past 10 years Mar. Drugs 2020, 18, 43 15 of 23 (2009–2019). Cluster analysis demonstrated that these works were still dispersive (these larger dots and crosses don't overplay and combine) and did not form a very concentrated research direction. 2.4.For Trendsexample, in Research these oninvestigations MAAs in Marine mainly Macroalgae included effects of ultraviolet radiation, nitrogen, temperature and climate change on MAAs contents and composition, the physiological activity and Figure7 shows a cluster view of studies about MAAs in marine macroalgae in the past 10 years seasonal variation of MAAs, MAAs profile and distribution, and so on. And five clusters formed (＃ (2009–2019). Cluster analysis demonstrated that these works were still dispersive (these larger dots 0-＃4) presented some researches about MAAs can cluster in these several areas. It was very clear and crosses don’t overplay and combine) and did not form a very concentrated research direction. that the preparation and purification of MAAs in marine macroalgae did not catch enough attention For example, these investigations mainly included effects of ultraviolet radiation, nitrogen, temperature of researchers in these studies between 2009 and 2019. and climate change on MAAs contents and composition, the physiological activity and seasonal MAAs were multi-functional compounds, namely included UV-photoprotective activity [54], variation of MAAs, MAAs profile and distribution, and so on. And five clusters formed (#0-#4) antioxidant properties [91,119], and other possible activities, such as anti-desiccant, protective agents presented some researches about MAAs can cluster in these several areas. It was very clear that against temperature variations [120], and etc [23,27–31]. Therefore, MAAs could be widely used in the preparation and purification of MAAs in marine macroalgae did not catch enough attention of food, cosmetics, and medicine in the future [97]. Note that in this application, it becomes very researchers in these studies between 2009 and 2019. important to study the preparation and purification of MAAs.

Figure 7. Cluster view of MAAs studies in marine algae between 2009 and 2019. Data extracted from Figure 7. Cluster view of MAAs studies in marine algae between 2009 and 2019. Data extracted from related studies collected in Web of Science. related studies collected in Web of Science. MAAs were multi-functional compounds, namely included UV-photoprotective activity [54], antioxidantIn fact, propertiesthe extraction [90, 118of MAAs], and otherin marine possible macroalgae activities, has such been as involved anti-desiccant, in many protective studies agentswhich againstwere mainly temperature concentrated variations on the [119 distribution], and etc. [[64,69,93,96,115],23,27–31]. Therefore, profile MAAs [120], couldphysiological be widely activity used in[55,67,71,104,121–124], food, cosmetics, and properties medicine in[56,82,93,125,126], the future [96]. Notechemical that characterization in this application, [54] it of becomes MAAs veryand importanteffects of some to study environment the preparation factors and on purificationMAAs [36,54,66,74,80,81,87,102–104,110,126,127]. of MAAs. However, furtherIn their fact, isolation the extraction and purification of MAAs did in marine not conduct. macroalgae has been involved in many studies whichUntil were now, mainly there concentrated were few studies on the on distribution the isolation, [64 purification,,69,92,95,114 ],and profile preparation [119], physiological of MAAs in activitymarine macroalgae. [55,67,71,103 Six,120 novel–123], mycosporine-like properties [56,81, 92amino,124, 125acids,], chemical bostrychines characterization A–F, were obtained [54] of MAAs from andBostrychia effects scorpioides of some environment [71]. A new factors MAA on catenelline MAAs [36 was,54,66 isolated,74,79,80 from,86,101 Catenella–103,109 repens,125, 126[49].]. However,MAAs in furtherChondrus their crispus isolation [57], and Palmaria purification palmata did [57], not conduct.Porphyra dioica [57], Porphyra haitanensis [127] and RhodymeniaUntil now, pseudopalmata there were [104] few have studies been on separated the isolation, and identi purification,fied. The and preparation preparation of porphyra-334 of MAAs in marinein Bangia macroalgae. atropurpurea Six [47], novel Eucheuma mycosporine-like [128], Gracilaria amino changii acids, [95], bostrychines Porphyra vietnamensis A–F, were obtained [78], Porphyra from Bostrychia scorpioides [71]. A new MAA catenelline was isolated from Catenella repens [49]. MAAs in Chondrus crispus [57], Palmaria palmata [57], Porphyra dioica [57], Porphyra haitanensis [126] and Rhodymenia pseudopalmata [103] have been separated and identified. The preparation of porphyra-334 in Bangia atropurpurea [47], Eucheuma [127], Gracilaria changii [94], Porphyra vietnamensis [78], Porphyra yezoensis [128], and Rhodymenia pseudopalmata [103] has been reported. Isolation and purification of others MAAs in Agarophyton chilense [104], Ahnfeltiopsis devoniensis [39,129], Bostrychia scorpioides [76,77], Champia novae-zelandiae [104], Chlamydomonas hedlyei [123], Chondracanthus chamissoi [50], Chondrus Mar. Drugs 2020, 18, 43 16 of 23 crispus [41,57], Gelidium corneum [39,129], Gelidium lingulatum [50], Gracilaria changii [108,130], Gracilaria cornea [87], Mastocarpus stellatus [76,77], Palmaria decipiens [123], Palmaria palmata [57,131], Porphyra dioica [57], Porphyra rosengurttii [39,119], Porphyra sp. [32,131], Porphyra tenera [123,132], Porphyra yezoensis [76,77,105,128], Pyropia leucosticte [39] and Pyropia plicata [104], such as palythine, palythinol, shinorine, usujirene and etc., that were often used as standards for identification and quantification of MAAs, also have been researched. The extraction process of MAAs in Eucheuma [124,133], Gloiopeltis furcata [51], Gracilaria chilensis [105], Porphyra sp., [134,135], Porphyra haitanensis [135] and Porphyra yezoensis [136] has been pointed. Therefore, the purification and preparation of MAAs in marine macroalgae need to be explored in future studies.

3. Materials and Methods

3.1. Methods Utilizing data obtained from the Web of Science, Springer, Google Scholar, and CNKI, the reliable material sources of this systematic manuscript paper were obtained from literature published during the last thirty years. Further, to provide more explicit knowledge, the development tendency of the studies about MAAs in marine macroalgae has been analyzed by using CiteSpace (4.0) [60]. Corresponding data on MAAs in marine macroalgae was extracted from related studies collected using the Web of Science during 2009 and 2019 years.

3.2. Total MAAs Contents and Speciﬁc MAA Concentration In this work, total MAAs content and/or speciﬁc MAA concentration in each marine macroalgae species was not clearly listed, however, they were obtained using an online database (http://210.28.32. 218/MAAs/), which was built by our team. A great deal of reports which were collected from the Web of Science, Springer, Google Scholar, and CNKI were built for this database.

4. Conclusions This review summed up the basic situation of MAAs in 572 species of marine macroalgae which belonged to 28 orders, from 1990 to 2019, in particular, 45 species in Chlorophyta, 41 species in Phaeophyta, and 486 species in Rhodophyta, and found the existence of 22 fully characterized MAAs and a large number of unidentified MAA(s) in them. Five MAAs, namely shinorine, porphyra-334, palythine, asterina-330, and palythinol were the most common in Rhodophytes, followed by mycosporine-glycine, palythene, and usujirene. Among them, seven MAAs, including asterina-330, mycosporine-glycine, palythene, palythinol, porphyra-334, palythine, and shinorine, were found in Chlorophytes and Phaeophytes. In addition, so far, aplysiapalythine A, aplysiapaly thine B, catenelline, prasiolin and bostrychines A–F only have been found in Rhodophytes. According to different orders of marine macroalgae, the total MAAs contents in 12 species macroalgal Chlorophytes, 8 species macroalgal Phaeophytes and 323 species macroalgal Rhodophytes were pointed out in this work. Meanwhile, we detailed the structure, extinction coefficient, retention time, and maximum absorption wavelength of 10 common MAAs. Further, an open online database (http://210.28.32.218/MAAs/) for MAAs in 501 species of marine macroalgae was established on datas metioned above to quickly retrieve information related to MAAs in marine macroalgae since 1990. In this database, the source (field/culture) and collection site of marine macroalgae, total MAAs content, MAA type and/or content have been listed. Finally, the studies about MAAs in marine macroalgae were analyzed using CiteSpace considering the past 10 years, and the result demonstrated that the purification and preparation of MAA purified standards from marine macroalgae constitute a domain worthy to be penetratingly explored in future studies. In order to gain better knowledge about the current states and progress of MAAs in marine macroalgae, more reports have to be collected regarding MAAs from other sources of data. Overall, Mar. Drugs 2020, 18, 43 17 of 23 based on data from the last 30 years, our work provided more a comprehensive reference and fast inquiry about MAAs in marine macroalgae for relevant researchers.

Author Contributions: Software, Y.S.; investigation, N.Z. and X.Z.; data curation, N.Z.; writing—original draft preparation, Y.S.; writing—review and editing, Y.S. and J.Z.; visualization, Y.S. and N.Z.; supervision, L.G. and G.G.; project administration, Y.S. and S.D. All authors have read and agreed to the published version of the manuscript. Funding: This work was supported by the Open Project Program of State Key Laboratory of Food Science and Technology, Jiangnan University (SKLF-KF-201904); Supported by Natural Science Fund for Colleges and Universities in Jiangsu Province (19KJA430010); the Priority Academic Program Development of Jiangsu Higher Education Institutions; Special Foundation for Excellent Young Teachers and Principals Program of Jiangsu Province, China; and Postgraduate Research and Innovation Plan Project in Jiangsu Province (SJCX19_1002). Conﬂicts of Interest: The authors declare no conﬂict of interest.

References

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