Diatoms synthesize sterols by inclusion of animal and fungal genes in the plant pathway

Carmela Gallo,Emiliano Manzo,Genoveffa Nuzzo,Angela Sardo,Simone Landi,Angelo Fontana,Giuliana d’Ippolito

doi:10.1038/s41598-020-60993-5

Abstract

Diatoms are ubiquitous microalgae that have developed remarkable metabolic plasticity and gene diversification. Here we report the first elucidation of the complete biosynthesis of sterols in the lineage. The study has been carried out on the bloom-forming species Skeletonema marinoi and Cyclotella cryptica that synthesise an ensemble of sterols with chemotypes of animals (cholesterol and desmosterol), plants (dihydrobrassicasterol and 24-methylene cholesterol), algae (fucosterol) and marine invertebrates (clionasterol). In both species, sterols derive from mevalonate through cyclization of squalene to cycloartenol by cycloartenol synthase. The pathway anticipates synthesis of cholesterol by enzymes of the phytosterol route in plants, as recently reported in Solanaceae. Major divergences stem from reduction of Δ24(28) and Δ24(25) double bonds which, in diatoms, are apparently dependent on sterol reductases of fungi, algae and animals. Phylogenetic comparison revealed a good level of similarity between the sterol biosynthetic genes of S. marinoi and C. cryptica with those in the genomes of the other diatoms sequenced so far.

Highlights

Diatoms are ubiquitous microalgae that have developed remarkable metabolic plasticity and gene diversification
Four different Δ5-sterols, namely 24-methylene cholesterol, dihydrobrassicasterol, clionasterol and fucosterol were identified by standard comparison in the GC-MS profiles of C. cryptica (Fig. 1)
In analogy with phytosterol biosynthesis, we found sequences that correlate with plant SMO1 (Sm-TR11964, Sm-TR30213) and SMO2 (Sm-TR319) in S. marinoi, whereas the transcriptome of C. cryptica showed only one sequence for a putative SMO1 (Cc-TR32604)

Summary

Introduction

Diatoms are ubiquitous microalgae that have developed remarkable metabolic plasticity and gene diversification. The study has been carried out on the bloom-forming species Skeletonema marinoi and Cyclotella cryptica that synthesise an ensemble of sterols with chemotypes of animals (cholesterol and desmosterol), plants (dihydrobrassicasterol and 24-methylene cholesterol), algae (fucosterol) and marine invertebrates (clionasterol). In both species, sterols derive from mevalonate through cyclization of squalene to cycloartenol by cycloartenol synthase. The report is new but underlines the possible role of sterols to control cell survival during phytoplankton blooms Diatoms possess both plant (e.g. brassicasterol) and animal (e.g. cholesterol) sterols[32]. Post analysis of the molecular data, sterol profiling and comparison with other diatom species provides general significance to this study

Methods

Results

Conclusion