Furanoterpene Diversity and Variability in the Marine Sponge Spongia officinalis, from Untargeted LC–MS/MS Metabolomic Profiling to Furanolactam Derivatives
Abstract
:1. Introduction
2. Results and Discussion
2.1. Untargeted Metabolomic Profiles of S. officinalis
2.2. Signals Involved in the Metabolomic Clustering
2.3. Compound Annotation through LC–MS/MS and Molecular Networking
- −
- Compound 1 was assigned to the linear furanosesterterpene demethylfurospongin-4, previously isolated from S. officinalis [12]. Its identification was confirmed by NMR on the isolated compound (Figures S5 and S6, Table S4). Therefore, the main cluster produced by molecular networking was assigned to the furanoterpene family.
- −
- Compound 2 was not observed in the network due to in-source fragmentation in positive ion mode.
- −
- Compounds 3, 4 and 5 did not appear in the furanoterpene cluster and appeared structurally unrelated. No structure could be proposed for compounds 3 and 4 based on their molecular masses and fragmentation patterns (Figure S7A,B). Compound 5 displayed a molecular formula and MS/MS spectra consistent with the coconut diethanolamide (C11 DEA), a synthetic surfactant considered as marine pollutant (Figure S7C) [22].
- −
- Compound 6 had no match in MarinLit as a furanoterpene molecule based on its assigned molecular formula C22H33NO3 and MS/MS spectrum (Figure S8A).
- −
- Compounds 7 and 8 were assigned to the molecular formula C21H28O3, which matched with two molecules previously isolated from Spongia spp.: furospongenone [23] and dihydrofurospongin-2 [25]. The intense m/z 135 and the m/z 179 product ions observed for compound 7 were consistent with the structure of dihydrofurospongin-2 (Figure S9A). The corresponding node was thus annotated as a dihydrofurospongin-2 type. The MS/MS spectrum of compound 8 displayed a small product ion at m/z 135, together with a species at m/z 149 (Figure S9B). This compound was proposed to contain a dimethyl-allyl backbone, but could not be further identified.
- −
- Compounds 9 and 10 were assigned to the molecular formula C21H30O5 corresponding to a series of furanoterpene isomers isolated from S. officinalis, named butenolide furospongin-1 [24]. These compounds contain a furan moiety and either a γ-hydroxy-α-β-butenolide or a β-γ-epoxy butenolide moiety. The fragmentation patterns of compound 9 in positive and negative ion modes (Figure S10A,B) were compatible with butenolide furospongin-1. The chromatographic peak corresponding to this compound had a bimodal peak shape, suggesting a close elution of two isomers. The fragmentation pattern of compound 10 seemed close to that of compound 9, although much weaker, in particular in positive ion mode (Figure S10C,D). In the literature, no difference in the fragmentation pattern of butenolide furospongin-1 has been reported when a γ-hydroxy-α-β-butenolide is replaced by a β-γ-epoxy butenolide [24], hindering unambiguous identification of compounds 9 and 10.
- −
- Compound 11 was assigned to the molecular formula C21H30O3, which could correspond to different furanoterpernes isolated from species of the Spongiidae family: furospongin-1 [9], tetrahydrofurospongin-2 [25] and furospongenol [23]. The product ions detected in the MS/MS spectrum of the [M + H]+ species of this compound (Figure S11) was compatible with the three structures. NMR analysis of the purified compound permitted to assign it to furospongin-1 (Figures S12 and S13, Table S5).
- −
- LC–MS/MS analysis revealed that compound 12 was in fact a mixture of two isomers showing distinct fragmentation patterns, and thus featured into two independent clusters (Figure 4c,d). These compounds were therefore named 12a and 12b. Their molecular formula C23H33NO5 had no match in MarinLit as a furanoterpene molecule.
- −
- The molecular formula C22H32O5 assigned to compound 13 (Table S2, Figure S8B) matched with irciformonins B and J isolated from Ircinia formosana [28,29]. The compound fragmentation pattern was consistent with the structure of irciformonin B.
- −
- Compounds 14 and 15, assigned to the molecular formulas C27H41NO5 and C28H33NO4, respectively, appeared outside the furanoterpene cluster. However, their fragmentation patterns included the diagnostic ion m/z 135 which could imply their annotation as furanoterpenes with unusual product ions (Figure S8C,D).
2.4. Structure Elucidation of New Furanoterpene Derivatives
2.5. Unravelling Pyrrolofuranoterpene Derivatives from S. officinalis
2.6. Metabolite Variability and Furanoterpene Signature
3. Materials and Methods
3.1. Materials
3.2. Sponge Extraction
3.3. LC–MS Analyses
3.4. NMR Analysis
3.5. Molecular Networking and Manual Dereplication
LC–MS/MS data were converted into mgf files using MassHunter® software,(Qualitative Analysis B.07.00, Agilent Technologies, Les Ulis, France). Converted data files were subjected to online GNPS workflow (http://gnps.ucsd.edu). Consensus spectra were generated through MS-Cluster with a parent ion mass tolerance of 0.5 Da and a fragment ion mass tolerance of 0.5 Da, with a minimum of 2 spectra. The networks were generated using the following settings: min pair cos: 0.7, minimum matched fragment ion: 6, network topK: 10. Resulting networks were visualized using Cytoscape 3.2.0. The preferred layout was applied. Node colors were mapped based on the source files of MS/MS spectra. The edge thickness attribute was defined to reflect cosine similarity scores, with thicker lines indicating higher similarity. Manual dereplication was performed using the MarinLit database (http://pubs.rsc.org/marinlit).
3.6. Multivariate Data Analysis
3.7. Compound Isolation and Characterization
4. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Compound | Retention Time (min) | m/z | Identification/Annotation | Reference |
---|---|---|---|---|
1 | 39.1 | 415.2 | Demethylfurospongin-4 | [12] |
2 | 32.5 | 433.3 | Furofficin, new compound | this study |
3 | 43.3 | 445.3 | Unknown | - |
4 | 36.3 | 568.4 | Unknown | - |
5 | 33.1 | 288.3 | Coconut C11 diethanolamide (a) | [22] |
6 | 33.4 | 360.3 | Furanoterpene, C22H33NO3 | - |
7 | 31.0 | 329.2 | Dihydrofurospongin-2 (a) | [23] |
8 | 42.1 | 329.2 | Furanoterpene, C21H28O3 | - |
9 | 32.8 | 363.2 | Isomers of γ-hydroxy-α,β-butenolide or β-γ-epoxy butenolide furospongin-1 (a) | [24] |
10 | 35.9 | 363.2 | Furanoterpene, C21H30O5 | - |
11 | 41.5 | 331.2 | Furospongin-1 | [9,23,25] |
12 | 31.8 | 404.2 | Two new isomers: Spongialactam A (12a) and Spongialactam B (12b) | this study |
13 | 36.7 | 377.2 | Irciformonin B (a) | - |
14 | 37.0 | 460.3 | Furanoterpene, C27H41NO5 | - |
15 | 29.8 | 448.3 | Furanoterpene, C28H33NO4 | - |
Furofficin (2) | Spongialactam A (12a) | Spongialactam B (12b) | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
δCa | δH (mult, J in Hz) | COSY | HMBC (1H͢͢-13C) | δCa | δH (mult, J in Hz) | COSY | HMBC (1H͢͢-13C) | δCa | δH (mult, J in Hz) | COSY | HMBC (1H͢͢-13C) | |
1 | 143.6 | 7.38 (dd, 1.7 ; 1.7) | 2, 4 | 2, 3, 4 | 143.7 | 7.37 (t, 1.7) | 2,4 | 3, 4 | 143.7 | 7.37 (t, 1.7) | 2, 4 | 2, 3, 4 |
2 | 111.6 | 6.30 (dd, 1.7 ; 0.7) | 1, 4 | 1, 3, 4 | 112,0 | 6.31 (bd 0.9) | 1, 4 | 1, 4 | 111.8 | 6.29 (bd, 0.9) | 1, 4 | 1, 4 |
3 | 126.0 | - | - | - | 126.05* | - | - | - | 126.4* | - | - | - |
4 | 139.8 | 7.27 (dd, 1.5 ; 0.9) | 1, 2, 5 | 2, 3, 1 | 140.0 | 7.25 (quint, 0.8) | 1, 2, 5 | 1, 2 | 139.9 | 7.25 (m) | 1, 2, 5 | 1, 2, 3 |
5 | 25.9 | 2.42 (brt, 7.4) | 4, 6 | 2, 3, 4, 6, 7 | 25.8 | 2.46 (t, 7.4) | 4, 6 | 2, 3, 6, 7 | 25.7 | 2.40 (t, 7.4) | 4, 6 | 2, 3, 4, 6, 7 |
6 | 25.3 | 1.60 (m) | 5, 7 | 5, 7 | 29.5 | 2.27 (m) | 5, 7 | 7 | 28.5 | 1.59 (m) | 5, 7 | 7 |
7a | 41.8 | 1.48 (m) | 6 | 8, 9 | 127.8 | 5.21 (bt, 7.1) | 6 | 9, 10 | 38.5 | 1.21 (m) | 6, 7b | - |
7b | 1.32 (m) | 6, 7a, 9 | - | |||||||||
8 | 72.8 | - | - | - | 133.9* | - | - | - | 29.9 | 1.71 (m) | 9, 10a | - |
9 | 26.5 | 1.13 (s) | - | 7, 8, 10 | 16.5 | 1.61 (brs) | 7 | 7, 8, 10 | 19.5 | 0.89 (d, 6.6) | 7b, 8 | 7, 8, 10 |
10a | 42.3 | 1.45 (m) | 11 | 7, 8, 9, 11, 12 | 50.0 | 2.05 (dd, 13.5 ; 6.3) | 10b, 11 | 7, 8, 9, 11 | 45.2 | 1.14 (ddd, 13.8, 9.8, 3.5) | 10b, 11 | - |
10b | 2.15 (dd, 13.1 ; 6.8) | 10a, 11 | 7, 8, 9, 11, 12 | 1.37 (ddd, 14.3, 9.5, 3.9) | 10a, 11 | - | ||||||
11 | 23.2 | 2.00 (m) | 10, 12 | 10, 12, 13 | 68.1 | 3.76 (m) | 10a, 10b, 12a | - | 68.0 | 3.77 (m) | 10, 12 | 11 |
12a | 125.4 | 5.15 (td, 7.1 ; 1.0) | 11, 14 | 11, 14, 15 | 45.4 | 1.13 (ddd, 14.1 ; 10.0 ; 3.4) | 11, 12b | - | 49.7 | 2.06 (dd, 13.3, 6.3) | 11, 12b | 11, 13, 14, 15 |
12b | 1.36 (ddd, 13.9 ; 9.9 ; 3.9) | 12a, 13 | - | 2.14 (dd, 13.4, 7.6) | 11, 12a | 10, 11, 13, 14, 15 | ||||||
13 | 135.5b | - | - | - | 30.1 | 1.72 (m) | 12b, 14 | - | 134.2b | - | - | - |
14 | 15.6 | 1.61 (brs) | 12 | 12, 13, 15 | 19.5 | 0.88 (d, 6.6) | 13 | 12, 13, 15 | 16.1 | 1.63 (brs) | 15, 16 | 12, 13, 15 |
15a | 40.4 | 2.05 (m) | 16 | 12, 13, 14, 16, 17 | 38.8 | 1.24 (m) | 15b, 13 | - | 127.2 | 5.21 (m) | 14, 16 | - |
15b | 1.34 (m) | 15a | - | |||||||||
16 | 28.8 | 2.35 (m) | 15, 17 | 13, 15, 17, 18 | 26.2 | 1.58 (m) | 17 | - | 27.0 | 2.29 (m) | 15 | 13, 15, 17 |
17 | 129.5 | 5.31 (t) | 16 | 15, 16, 19, 20 | 27.0 | 2.24 (m) | 16, 20, 21 | 18, 20 | 26.8 | 2.30 (m) | 20, 21 | 16, 18, 19, 20 |
18 | 140.2b | - | - | - | 140.1b | - | - | - | 138.2b | - | - | - |
19 | 177.5b | - | - | - | 173.8b | - | - | - | 173.8b | - | - | - |
20 | 35.3 | 2.31 (m) | 21, 22 | 21 | 137.7 | 6.83 (m) | 17, 21 | 19, 21 | 137.9 | 6.83 (m) | 17, 21 | 19, 21 |
21 | 28.9 | 2.29 (m) | 20, 22, 24 | 20 | 53.0 | 4.06 (d, 1.7) | - | 18, 20 | 53.0 | 4.05 (d, 1.6) | 17, 20 | 18, 20 |
22 | 139.2 | 6.61 (td, 8.7 ; 1.6) | 20, 21, 24 | 24 | 46.7 | 4.05 (brs) | - | 19, 21, 23 | 46.9 | 4.03 (brs) | - | 19, 21, 23 |
23 | 129.9b | - | - | - | 175.5b | - | - | - | 175.9b | - | - | - |
24 | 13.0 | 1.81 (brs) | 21, 22 | 22, 23, 25 | ||||||||
25 | 174.9b | - | - | - |
- a
- 13C assignments supported by HSQC experiment.
- b
- 13C assignments supported by HMBC experiment.
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Bauvais, C.; Bonneau, N.; Blond, A.; Pérez, T.; Bourguet-Kondracki, M.-L.; Zirah, S. Furanoterpene Diversity and Variability in the Marine Sponge Spongia officinalis, from Untargeted LC–MS/MS Metabolomic Profiling to Furanolactam Derivatives. Metabolites 2017, 7, 27. https://doi.org/10.3390/metabo7020027
Bauvais C, Bonneau N, Blond A, Pérez T, Bourguet-Kondracki M-L, Zirah S. Furanoterpene Diversity and Variability in the Marine Sponge Spongia officinalis, from Untargeted LC–MS/MS Metabolomic Profiling to Furanolactam Derivatives. Metabolites. 2017; 7(2):27. https://doi.org/10.3390/metabo7020027
Chicago/Turabian StyleBauvais, Cléa, Natacha Bonneau, Alain Blond, Thierry Pérez, Marie-Lise Bourguet-Kondracki, and Séverine Zirah. 2017. "Furanoterpene Diversity and Variability in the Marine Sponge Spongia officinalis, from Untargeted LC–MS/MS Metabolomic Profiling to Furanolactam Derivatives" Metabolites 7, no. 2: 27. https://doi.org/10.3390/metabo7020027
APA StyleBauvais, C., Bonneau, N., Blond, A., Pérez, T., Bourguet-Kondracki, M. -L., & Zirah, S. (2017). Furanoterpene Diversity and Variability in the Marine Sponge Spongia officinalis, from Untargeted LC–MS/MS Metabolomic Profiling to Furanolactam Derivatives. Metabolites, 7(2), 27. https://doi.org/10.3390/metabo7020027