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Octocoral_briarane_FBMN_A widespread natural product gene cluster family to briarane diterpenoids in coral animals

ABSTRACT: Soft corals are unique amongst animals in their prolific production of bioactive terpenoid natural products that rival the chemical diversity of plants and microbes. We recently established that octocorals uniformly express terpene cyclases and that their encoding genes often reside within putative biosynthetic gene clusters, a feature uncommon in animal genomes. In this work, we report the discovery and characterization of a widespread gene cluster family for the biosynthesis of briarane diterpenoids that number over 600 molecules distinct to corals. We sequenced five genomes from evolutionarily discrete families of briarane-producing octocorals, including the chromosomally resolved precious coral Corallium rubrum, and identified a common five-gene cluster composed of a terpene cyclase, three cytochrome P450s, and a short-chain dehydrogenase. Using Escherichia coli and Saccharomyces cerevisiae as hosts and homologous briarane biosynthesis genes from seven corals, we reconstituted the biosynthesis of cembrene B g-lactone, which contains the g-lactone structural feature distinctive of briarane diterpenoids. The discovery of the genomic basis of briarane biosynthesis not only allows for its biological examination across coral species but establishes that animals, like microbes and plants, also employ gene cluster families to produce specialized metabolites.

INSTRUMENT(S): 6530A Q-TOF LC/MS

ORGANISM(S): Corallium Rubrum (ncbitaxon:142104) Dichotella Gemmacea (ncbitaxon:767270) Renilla Koellikeri (ncbitaxon:6135) Stylatula Elongata (ncbitaxon:1214922) Briareum Asbestinum (ncbitaxon:86543) Erythropodium Caribaeorum (ncbitaxon:86550)

SUBMITTER: Bradley Moore

PROVIDER: MSV000094792 | MassIVE | Fri May 17 15:50:00 BST 2024

REPOSITORIES: MassIVE

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Project description:Purpose: Corals are major sources of dimethylsulphoniopropionate (DMSP), a compound that plays a central role in the global sulphur cycle. While DMSP biosynthesis pathways have been investigated in plants and algae, the molecular basis for its production by corals is unknown. Given its potential role as an osmolyte, the effect of salinity stress on levels of DMSP was investigated in both adults and juveniles (lacking photosynthetic symbionts) of the coral Acropora millepora. This study used transcriptomic data to analyse the effects of salinity over the coral A. millepora and to identify coral genes likely to be involved in DMSP biosynthesis. Methods: Adults coral transcriptomic libraries were constructed from samples exposed during 1 and 24 hours of salinity treatment (25 PSU) and control (35 PSU) conditions (n=5 per condition). Juveniles coral transcriptomic libraries were constructed from samples exposed to 24 and 48 hours of salinity treatment (28 PSU) and control (35 PSU) conditions (n=6 per condition). All libraries were sequenced by 100 bp paired-end in a HiSeq 2000. Reads were mapped onto the Acropora millepora genome using TopHat2 to produce a count data gene expression matrix for subsequent gene expression analysis using DESeq2 package. Results: In adult coral samples, 5.5 - 10.2 million RNAseq reads were obtained for each treatment sampling time while 3.4 - 8.8 million reads were obtained for each juvenile coral sample. The count matrix of the 26,622 A. millepora gene predictions were generated using htseq-count workflow. BlastP analysis of the A. millepora gene predictions led to the identification of coral members of gene families implicated in DMSP biosynthesis in other organisms, while RNA-seq data was used to identify the differentially expressed ones in response to hyposaline stress and on this basis were considered to be candidates for roles in DMSP biosynthesis in corals. Conclusions: Hyposaline stress increased DMSP production in both adults and aposymbiotic juvenile corals, and transcriptomic analyses highlighted the potential involvement of specific candidate genes in the production of DMSP via an alga-like pathway. The biochemistry of DMSP production is not well established for any eukaryotic system and, as the first animals in which it has been demonstrated, this is particularly true in the case of corals. Our RNA-seq results enabled the identification of candidates for roles in DMSP biosynthesis in corals but, given its critical roles in diverse biological processes, a thorough investigation of the molecular mechanisms leading to its production by corals is required.

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Octocoral_briarane_FBMN_A widespread natural product gene cluster family to briarane diterpenoids in coral animals

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