Abstract
Ascidians and their associated microbiota are prolific producers of bioactive marine natural products. Recent culture-independent studies have revealed that the tunic of the solitary ascidian Ciona intestinalis (sea vase) is colonized by a diverse bacterial community, however, the biotechnological potential of this community has remained largely unexplored. In this study, we aimed at isolating the culturable microbiota associated with the tunic of C. intestinalis collected from the North and Baltic Seas, to investigate their antimicrobial and anticancer activities, and to gain first insights into their metabolite repertoire. The tunic of the sea vase was found to harbor a rich microbial community, from which 89 bacterial and 22 fungal strains were isolated. The diversity of the tunic-associated microbiota differed from that of the ambient seawater samples, but also between sampling sites. Fungi were isolated for the first time from the tunic of Ciona. The proportion of bioactive extracts was high, since 45% of the microbial extracts inhibited the growth of human pathogenic bacteria, fungi or cancer cell lines. In a subsequent bioactivity- and metabolite profiling-based approach, seven microbial extracts were prioritized for in-depth chemical investigations. Untargeted metabolomics analyses of the selected extracts by a UPLC-MS/MS-based molecular networking approach revealed a vast chemical diversity with compounds assigned to 22 natural product families, plus many metabolites that remained unidentified. This initial study indicates that bacteria and fungi associated with the tunic of C. intestinalis represent an untapped source of putatively new marine natural products with pharmacological relevance.
Highlights
Marine organisms are highly valuable sources for bioactive natural products (NPs) [1,2] and have yielded about 30,000 compounds so far [3]
69 tunic-associated strains were cultivated on 2 different media: bacteria were grown on glucose-yeast-malt (GYM) [43] and MB media while the fungal isolates were grown on casamino-acids-glucose (CAG) [44] and PDA media
111 bacterial and fungal isolates were obtained from the tunic of C. intestinalis and 101 from seawater references sampled at two sites (Figure 1a, Table S2)
Summary
Marine organisms are highly valuable sources for bioactive natural products (NPs) [1,2] and have yielded about 30,000 compounds so far [3]. The polyketide arenimycin that inhibits multidrug-resistant Staphylococcus aureus [19] is only one out of several antibiotics produced by actinobacteria associated with E. turbinata [16,20,21] Another example is trichodermamide B, an antimicrobial and cytotoxic dipeptide that was isolated from the Didemnum molle–associated fungus Trichoderma virens [22]. Previous culture-independent microbiome studies have demonstrated a broad bacterial diversity associated with the tunic of Ciona spp. The gammaproteobacterium Pseudoalteromonas tunicata represents the only example of a tunic-associated bacterial isolate from C. intestinalis producing metabolites with antibacterial and antifouling activities [31,32]. As ascidian-associated microbes have previously yielded novel metabolites with promising antibiotic and anticancer activities, the organic extracts of tunic-derived strains were tested against a panel of human pathogens (bacteria and fungi) and cancer cell lines. By employing the bioactivity and chemical diversity as main filters, several promising extracts were prioritized for in-depth chemical studies in future
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