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

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.

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  MAAs have been found in 45 species of the green algae in Chlorophyta [2][3][4][5]7,35,64]. Among them, total MAAs contents were determinied in only 12 species. The green algae with high total MAAs contents belong to Prasiolales, and contents were more than 3.5 mg/g DW (Figure 3a), such as Prasiola crispa ssp. antarctica [3], Prasiola crispa collected from South Shetlands [40] and Kongsfjorden [35] respectively. The total MAAs contents in other macroalgal Chlorophytes were very low, with values ranging between 0.0045 and 0.275 mg/g DW. Therefore, some bars which represent the total MAAs contents in different marine Chlorophytes were almost on the ordinate.
The specific parameters of 10 types of MAAs in marine macroalgae, such as structure, extinction coefficient, retention time and maximum absorption wavelength, have been showed in Table 1. Unfortunately, some parameters of these MAAs have not been determined, for instance, the extinction coefficient of mycosporine-2-glycine and usujirene. This should be due to the lack of commercially available MAAs standards. Table 1. Structure, molar extinction coefficient, retention time, and maximum absorption wavelength of MAAs in marine macroalgae [43,95]. In addition, it is worth mentioning that the difference of the total MAAs or MAA value between cultivated marine macroalgae and field material existed from same collection location. For exsample, cultured Stictosiphonia tangatensi [40] exhibited only 47.8% of the total MAAs found in the field sample [5]. Chondrus crispus, which in culture esposured to green or blue light radiation, exhibited asterina-330, palythene, palythinol and shinorine that were lack of MAAs in the field sample. Similary phenomenons also occurred in other seaweeds, such as Bostrychia radicans [5,40], Caloglossa stipitata [5,49], Chondrus crispus [60,72], Kallymenia antarctica [3], Mazzaella laminarioides [74], Neuroglossum ligulatum [3], Palmaria decipiens [3], Plocamium cartilagineum [3], Porphyra columbina [6,43], and Porphyra endiviifolium [3]. In the database that we set up later, we made clear the source of marine macroalgae that was field or culture, or commercial provision.
The specific parameters of 10 types of MAAs in marine macroalgae, such as structure, extinction coefficient, retention time and maximum absorption wavelength, have been showed in Table 1. Unfortunately, some parameters of these MAAs have not been determined, for instance, the extinction coefficient of mycosporine-2-glycine and usujirene. This should be due to the lack of commercially available MAAs standards. Table 1. Structure, molar extinction coefficient, retention time, and maximum absorption wavelength of MAAs in marine macroalgae [43,94].
The specific parameters of 10 types of MAAs in marine macroalgae, such as structure, extinction coefficient, retention time and maximum absorption wavelength, have been showed in Table 1. Unfortunately, some parameters of these MAAs have not been determined, for instance, the extinction coefficient of mycosporine-2-glycine and usujirene. This should be due to the lack of commercially available MAAs standards. Table 1. Structure, molar extinction coefficient, retention time, and maximum absorption wavelength of MAAs in marine macroalgae [43,95]. In addition, it is worth mentioning that the difference of the total MAAs or MAA value between cultivated marine macroalgae and field material existed from same collection location. For exsample, cultured Stictosiphonia tangatensi [40] exhibited only 47.8% of the total MAAs found in the field sample [5]. Chondrus crispus, which in culture esposured to green or blue light radiation, exhibited asterina-330, palythene, palythinol and shinorine that were lack of MAAs in the field sample. Similary phenomenons also occurred in other seaweeds, such as Bostrychia radicans [5,40], Caloglossa stipitata [5,49], Chondrus crispus [60,72], Kallymenia antarctica [3], Mazzaella laminarioides [74], Neuroglossum ligulatum [3], Palmaria decipiens [3], Plocamium cartilagineum [3], Porphyra columbina [43,79], and Porphyra endiviifolium [3]. In the database that we set up later, we made clear the source of marine macroalgae that was field or culture, or commercial provision.
The specific parameters of 10 types of MAAs in marine macroalgae, such as structure, extinction coefficient, retention time and maximum absorption wavelength, have been showed in Table 1. Unfortunately, some parameters of these MAAs have not been determined, for instance, the extinction coefficient of mycosporine-2-glycine and usujirene. This should be due to the lack of commercially available MAAs standards. Table 1. Structure, molar extinction coefficient, retention time, and maximum absorption wavelength of MAAs in marine macroalgae [43,95].  In order to clearly present 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 and 3 are presenteed. In these two tables, all marine macroalgae were grouped according to the types of MAAs that they contained. In order to clearly present 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 and 3 are presenteed. In these two tables, all marine macroalgae were grouped according to the types of MAAs that they contained. In order to clearly present 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 and 3 are presenteed. In these two tables, all marine macroalgae were grouped according to the types of MAAs that they contained.

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.

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 ( Figure 6) and its numbers were more than 100 species (Table 4) in the past 30 years. From Figure 6 it appeared that marine macroalgae with no detectable MAA concentrations have a wide taxonomic distribution.
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. . 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. For example, these investigations mainly included effects of ultraviolet radiation, nitrogen, temperature and climate change on MAAs contents and composition, the physiological activity and seasonal variation of MAAs, MAAs profile and distribution, and so on. And five clusters formed (#0-#4) presented some researches about MAAs can cluster in these several areas. It was very clear that the preparation and purification of MAAs in marine macroalgae did not catch enough attention of researchers in these studies between 2009 and 2019. [114,118]. These studies were not included in this paper. Figure 7 shows a cluster view of studies about MAAs in marine macroalgae in the past 10 years (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. For example, these investigations mainly included effects of ultraviolet radiation, nitrogen, temperature and climate change on MAAs contents and composition, the physiological activity and seasonal variation of MAAs, MAAs profile and distribution, and so on. And five clusters formed (＃ 0-＃4) presented some researches about MAAs can cluster in these several areas. It was very clear that the preparation and purification of MAAs in marine macroalgae did not catch enough attention of researchers in these studies between 2009 and 2019.

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.

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.

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, 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.