Furanoterpene Diversity and Variability in the Marine Sponge Spongia officinalis, from Untargeted LC–MS/MS Metabolomic Profiling to Furanolactam Derivatives

Abstract

The Mediterranean marine sponge Spongia officinalis has been reported as a rich source of secondary metabolites and also as a bioindicator of water quality given its capacity to concentrate trace metals. In this study, we evaluated the chemical diversity within 30 S. officinalis samples collected over three years at two sites differentially impacted by anthropogenic pollutants located near Marseille (South of France). Untargeted liquid chromatography—mass spectrometry (LC–MS) metabolomic profiling (C18 LC, ESI-Q-TOF MS) combined with XCMS Online data processing and multivariate statistical analysis revealed 297 peaks assigned to at least 86 compounds. The spatio-temporal metabolite variability was mainly attributed to variations in relative content of furanoterpene derivatives. This family was further characterized through LC–MS/MS analyses in positive and negative ion modes combined with molecular networking, together with a comprehensive NMR study of isolated representatives such as demethylfurospongin-4 and furospongin-1. The MS/MS and NMR spectroscopic data led to the identification of a new furanosesterterpene, furofficin (2), as well as two derivatives with a glycinyl lactam moiety, spongialactam A (12a) and B (12b). This study illustrates the potential of untargeted LC–MS metabolomics and molecular networking to discover new natural compounds even in an extensively studied organism such as S. officinalis. It also highlights the effect of anthropogenic pollution on the chemical profiles within the sponge.

An Anti-Inflammatory 2,4-Cyclized-3,4-Secospongian Diterpenoid and Furanoterpene-Related Metabolites of a Marine Sponge Spongia sp. from the Red Sea

“…The IR spectrum displayed the absorptions of carboxylic acid (3105–2857 and 1708 cm –1 ) and olefin (1654 cm −1 ). The NMR data ( Table 2 ) showed the presence of a monosubstituted furan ring (δ C 142.5, CH; 138.8, CH; 111.0, CH; and 124.7, C; δ H 7.34, 7.20, and 6.27, each 1H, s) [ 24 , 25 , 26 , 42 ], a trisubstituted olefin (δ C 124.7, CH; δ H 5.22, 1H, s), a methyl (δ C 15.9; δ H 1.61, 3H, s) and a carbonyl group (δ C 180.0, C). Other 1 H NMR signals in the shielded region (δ H 2.25–2.47, 8H) were attributable to four methylene groups, as depicted from the COSY ( Figure 2 ) correlations.…”

“…Many natural products from sponges have been shown to exhibit a variety of biological activities, such as antimicrobial [ 2 , 3 , 4 , 5 ], antiviral [ 6 , 7 , 8 ], antiprotozoal [ 8 , 9 , 10 ], cytotoxic [ 6 , 11 , 12 , 13 ], anti-inflammatory [ 14 , 15 , 16 ], antioxidant [ 4 , 17 , 18 ], immunosuppressive [ 1 , 19 , 20 ], and antifeedant [ 21 , 22 , 23 ]. The genus Spongia (Spongidae) has been chemically investigated since 1971 [ 24 ] and the studies have led to the discovery of a series of furanoterpenes [ 24 , 25 , 26 ], spongian diterpenoids [ 27 , 28 , 29 , 30 , 31 , 32 ], scalarane sesterterpenoids [ 33 , 34 , 35 ], sesquiterpene quinones [ 36 , 37 ], along with other kinds of metabolites, for example, sterols [ 38 , 39 , 40 ] and macrolides [ 41 ].…”

Lipid Annotation by Combination of UHPLC-HRMS (MS), Molecular Networking, and Retention Time Prediction: Application to a Lipidomic Study of In Vitro Models of Dry Eye Disease

“…To elucidate the structure of unknown compounds, bioinformatics tools are strongly valuable. Among them, molecular networks (MNs) have recently been proposed, historically in the field of plant secondary metabolites, to identify compounds of biotechnological interest or exhibiting promising pharmacological activity [17][18][19][20]. Molecular networks are a computational strategy aimed at organizing and visualizing hundreds of molecules using their MS/MS spectra in accordance to their similarities through the assumption that structurally related molecules display similar product ion spectra [21].…”

Application of in situ Solid-Phase Microextraction on Mediterranean Sponges for Untargeted Exometabolome Screening and Environmental Monitoring

“…The microorganisms provide the host with secondary metabolites of important bioactivity, such as drugs that can overcome bacterial diseases to degradation metabolites of marine pollutants. The use of untargeted metabolomics profiling can provide insight into the complex metabolic variability within sponges and promote research toward the development of novel bioactive compounds with potential for pharmaceutical and industrial applications (Bauvais et al, 2017;Sauleau et al, 2017). In addition, this approach could complement traditional morphological and genetic approaches to classifying taxa (i.e., chemotaxonomy) (Ivanišević et al, 2011), as well as analyzing the sponge's physiological state and its response to environmental stressors or fluctuations (Cachet et al, 2015;Reverter et al, 2018).…”