Sinularia Sp Classification Essay

2.1. Selection and Quantification of Terpene/Sterol NMR Signals

Full assignment of the major NMR signals in coral secondary metabolites described herein was performed as detailed in our previous work using 1D (one-dimensional) NMR and 2D (two-dimensional) NMR experiments [18]. Nevertheless, for the quantification described herein using 1D NMR to be optimal, full relaxation of the protons of diterpene signals and the internal standard HMDS had to be achieved. For that, a rather large sum of relaxation delay and acquisition time of 23 s was employed for NMR acquisition, as the longest relaxation times were 4.5 s for the HMDS protons. For quantification, NMR signals unique to each metabolite, and also sufficiently separated from neighboring signals, were selected. Methyl signals were of premium preference as their large integration demarcates them readily from the noisy background set off by the many single protons derived from other, less abundant compounds (Figure 1). Figure 2 shows a representative 1H-NMR spectrum of Sarcophyton convolutum (SC1), with assigned NMR signals used for metabolite quantification as summarized in Suppl. Table S2. Quantified NMR signals belonged to one sesquiterpene viz. guaiacophine, four diterpenes viz. sarcophine, and one sterol viz. gorgosterol (Figure 1). For N1 guaiacophine, the signal of H3-14 (δH 1.13 ppm, d, J = 6.9 Hz) was used for quantification, being more intense than its olefinic proton H-6 (δH 6.26 ppm) and also better separated than H3-12 (δH 1.81 ppm) and H3-13 (δH 1.82 ppm) signals. The latter ones slightly overlapped with H3-17 (δH 1.79 ppm) present in diterpenes N2–N5 (Figure 2). Absence of N1 guaiacophine in some soft coral specimens was affirmed by the absence of its H3-14 and olefinic H-6 NMR signals as evident in Figure 2. The cembranoid diterpenes N2-N5 exhibit almost similar structural features (Figure 1), including a 14-membered macrocyclic sarcophine skeleton fused to a five-membered α,β-unsaturated-γ-lactone ring. With regard to structural differences, the diterpene enantiomers N2/3 exhibit an epoxy bridge between C7/C8, whereas the diastereomers N4/N5 are epimers with two vicinal hydroxyl groups at C7/C8. Consequently, the signal of H-7 in N2/3, N4, and N5 was used for quantification appearing at δ 2.63, 3.44, and 3.55 ppm, respectively. In detail, integration of the H-7 signal at δH 2.63 ppm was used to quantify N2/3 and to distinguish them from the diastereoisomeric pair N4/5. Analogously, the signals of H-7 appearing at δH 3.44 ppm and δH 3.55 ppm in N4 and N5 were used for their respective quantification. The steroid gorgosterol (N6) bears a characteristic cyclopropane ring in its side chain (a gorgostane-type side chain) and was quantified from its unique H-30a (δH 0.48 ppm & dd, J = 9, 4.2 Hz). In contrast, signal for H-30b was found to be interfering with other unknown protons. Although H3-27 signal (δH 0.80 ppm & d, J = 6 Hz) is quite distant from H3-15 in N1 (δH 0.89 ppm & d, J = 6 Hz), it was not used for quantification as it showed more than one crosspeak correlation in HSQC (data not shown). Consequently, signal of H-30a was used for quantification, despite its low signal/noise ratio when compared to its counterpart H3-27 (Figure S1). All other methyl group signals of H3-18, H3-19, H3-21, H3-26, H3-28, and H3-29 in N6 were not well resolved from those belonging to other diterpenes found in extract.

Sesquiterpenes are represented by guaiacophine (N1), which was found to occur at its highest levels of ca. 10 µg/mg mostly in S. convolutum (SC) and in one of the S. glaucum specimens (SG1) (Figure 3). Compared to the sesquiterpene “guaiacophine”, diterpenes (N2–5) form the major class of secondary metabolites in corals. The enantiomers sarcophine/ent-sarcophine (N2/3) were the most abundant diterpenes in samples of S. acutum (SA), S. convolutum (SC2), S. ehrenbergi (SE2-4), S. glaucum (SG), and S. regulare (SR1-3). Among the monitored metabolites, dihydroxydeepoxysarcophine diastereoisomers (N4/N5) and gorgosterol (N6) were the ones detected in all species examined (Figure 3). The highest levels of diterpene N4 were recorded in S. convolutum (SC1) and in an unidentified Sarcophyton sp. (S) at ca. 25.6 and 31 µg/mg, respectively, versus the lowest levels detected in the Lobophyton (LP) species (ca. 5.5 µg/mg). Interestingly, N5, a diastereomer of N4, showed a slightly different accumulation pattern to N4 with maximum levels observed in both S. glaucum (SG1) and S. convolutum (SC2) at ca. 33 µg/mg, and minimal abundance in S. ehrenbergi (SE4) at 4.6 µg/mg. Gorgosterol, a common sterol, was found at levels ranging from ca. 26 µg/mg in S. acutum (SR1) to almost being absent in Sinularia species (SP).

2.2. Multivariate Data Analysis of the Targeted Metabolite Profiling by qNMR of Soft Corals

Targeted metabolite analyses of the 16 soft coral specimens (Suppl. Table S1) were based on the quantifiable compounds (Figure 1). This allowed us to assess the heterogeneity among coral specimens and to compare it to the untargeted NMR approach reported earlier [18]. The two major principal components (PC1/PC2) accounted for ca. 85.8% of the total variance. The loading plot (Figure 4a) revealed that dihydroxydeepoxysarcophine and gorgosterol (N4-6) were most responsible for coral discrimination via PC1. Dihydroxydeepoxysarcophine and gorgosterol were both positively correlated to PC1. In contrast, guaiacophine (N1) and sarcophine/ent-sarcophine (N2/3) were associated with sample segregation along PC2. Sinularia and Lobophyton were clustered together on the negative side of PC1, suggesting that a targeted profiling approach, limited as it is, could readily discriminate them from Sarcophyton genus. Aquarium grown soft corals (SE4 and SG3) were clustered together on the negative side of PC1. The positive side of PC1 showed clustering of S. regulare sp. (SR1-3) individual specimens suggesting that the geographical impact on metabolite composition is not very strong in these species. In contrast, in case of either S. glaucum sp. (SG1-3) or S. ehrenbergi sp. (SE1-4) specimens, samples failed to cluster together.

Hierarchical cluster analysis (HCA) is an additional tool for revealing interrelationships among coral species. It also offers a more intuitive graphical way for result interpretation. HCA showed two clear clusters: group A comprised of six specimens, whereas group B included the remaining 10 soft coral specimens (Figure 4b). Group A showed a distinct subcluster (1A) of Sinularia and Lobophyton species that are chemically different from the rest of Sarcophyton sp., providing evidence for the validity of the employed targeted profiling approach for coral classification. Sinularia and Lobophyton species were included in the study as distant outliers to assess whether the multivariate data analysis model can effectively distinguish between various Sarcophyton sp. Group A also displayed a distinct sub-cluster (2A) constituted of the aquarium grown soft corals (SE4 and SG3). Similar to PCA results (Figure 4a), all specimens for either S. glaucum or S. ehrenbergi failed to cluster in one group (Figure 4b).

2.3. Cytotoxic Activity of Soft Corals

Soft coral ethyl acetate extracts subjected to NMR fingerprinting were further assessed for their in vitro cytotoxicity against human colon epithelium adenocarcinoma cell lines (HT29) and human prostate cancer cell lines (PC3). Both cell lines showed a comparable response towards S. ehrenbergi (SE2 & SE4), S. glaucum (SG1 & SG3), S. regulare (SR3), and Sinularia and Lobophyton species, with respective IC50 values of ca. 22, 33, 36, 60, 21, 8, and 9 µg/mL as shown in Figure 5. S. acutum, S. convolutum, S. glaucum (SG2), and S. regulare (SR1) displayed a stronger cytotoxic activity against HT29, while S. regulare (SR2) was more effective against PC3.

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