Sioxanthin, a novel glycosylated carotenoid, reveals an unusual subclustered biosynthetic pathway

Abstract

Summary Members of the marine actinomycete genus Salinispora constitutively produce a characteristic orange pigment during vegetative growth. Contrary to the understanding of widespread carotenoid biosynthesis pathways in bacteria, Salinispora carotenoid biosynthesis genes are not confined to a single cluster. Instead, bioinformatic and genetic investigations confirm that four regions of the S. tropica CNB-440 genome, consisting of two gene clusters and two independent genes, contribute to the in vivo production of a single carotenoid. This compound, namely (2’S)-1’-(β-D-glucopyranosyloxy)-3’,4’-didehydro-1’,2’-dihydro-φ,ψ-caroten-2’-ol, is novel and has been given the trivial name “sioxanthin”. Sioxanthin is a C40-carotenoid, glycosylated on one end of the molecule and containing an aryl moiety on the opposite end. Glycosylation is unusual amongst actinomycete carotenoids, and sioxanthin joins a rare group of carotenoids with polar and non-polar head groups. Gene sequence homology predicts that the sioxanthin biosynthetic pathway is present in all of the Salinispora as well as other members of the family Micromonosporaceae. Additionally, this study’s investigations of clustering of carotenoid biosynthetic genes in heterotrophic bacteria show that a non-clustered genome arrangement is more common than previously suggested, with nearly half of the investigated genomes showing a non-clustered architecture.

Genome Analysis of Two Pseudonocardia Phylotypes Associated with Acromyrmex Leafcutter Ants Reveals Their Biosynthetic Potential

“…Ps1 and Ps2 strains share two terpene encoding BGCs ( Figures 4B,D , clusters B and D), hydrocarbons comprised of isoprene-derived units that have diverse bioactivities including antimicrobial activity (Gershenzon and Dudareva, 2007; Gallucci et al, 2009). One of these terpene BGCs (cluster B) has similarity to carotenoid BGCs, and encodes a polyprenyl synthetase and a phytoene synthase (Richter et al, 2015), while the other shared terpene BGC (cluster D) contains a terpene cyclase closely related to a lycopene cyclase found in carotenoid biosynthesis. This cluster also has similarity to a conserved cluster in Rhodococcus bacteria.…”

The marine actinomycete genus Salinispora: a model organism for secondary metabolite discovery

“…While this was assumed to be due to carotenoid production, the biosynthetic origin and structures of these compounds had not been defined. A bioinformatic search of the S. tropica strain CNB-440 genome revealed genes associated with carotenoid biosynthesis in four distinct chromosomal regions 123 . Genetic investigations confirmed that, contrary to what is typically observed in bacteria, carotenoid biosynthesis in Salinispora spp.…”

Gene Flow and Molecular Innovation in Bacteria

“…Genome-mining efforts compensate for this deficiency. For example, the production of the glycosylated terpene sioxanthin from Salinispora tropica CNB-400 is dependent on four genetic loci[33], and a single promiscuous enzyme is required for glycosylation during the biosynthesis of a plecomacrolide and methyl-rhamnosylated phenazines in Kitasatospora sp. MBT166[34].…”