A Plastic Biosynthetic Pathway for the Production of Structurally Distinct Microbial Sunscreens

Mycosporine-like amino acids (MAAs) are small, colorless,and water-solublesecondary metabolites. They have high molar extinction coefficientsand a unique UV radiation absorption mechanism that make them effectivesunscreens. Here we report the discovery of two structurally distinctMAAs from the lichen symbiont strain Nostoc sp. UHCC0926. We identified these MAAs as aplysiapalythine E (C23H38N2O15) and tricore B (C34H53N4O15) using a combination ofhigh-resolution liquid chromatography-mass spectrometry (HR-LCMS)analysis and nuclear magnetic resonance (NMR) spectroscopy. We obtaineda 8.3 Mb complete genome sequence of Nostoc sp. UHCC0926 to gain insights into the genetic basis for the biosynthesisof these two structural distinct MAAs. We identified MAA biosyntheticgenes encoded in three separate locations of the genome. The organizationof biosynthetic enzymes in Nostoc sp. UHCC 0926 necessitatesa branched biosynthetic pathway to produce two structurally distinctMAAs. We detected the presence of such discontiguous MAA biosyntheticgene clusters in 12% of the publicly available complete cyanobacterialgenomes. Bioinformatic analysis of public MAA biosynthetic gene clusterssuggests that they are subject to rapid evolutionary processes resultingin highly plastic biosynthetic pathways that are responsible for thechemical diversity in this family of microbial sunscreens.

Automated summary

Two structurally distinct MAAs were identified in the lichen symbiont strain Nostoc sp. UHCC0926, and their biosynthesis in cyanobacteria was found to occur through a branched pathway. The presence of similar gene clusters in other cyanobacterial genomes suggests rapid evolutionary processes leading to chemical diversity in this family of microbial sunscreens.