Enhancing Solanine Production and Antifungal Activity by Streptomyces abikoensis XH-17 through Combined Ribosome Engineering and Post-Translational Modification

Abstract

Solanine, a strong poison alkaloid typically produced by staple food crops, such as sprouted potatoes, poses a potential risk to food safety, therefore, controlling solanine levels is one of the important targets for human health. Streptomyces species are ubiquitous across diverse environments and are acclaimed for their extensive production of bioactive compounds, including antibiotics, anticancer agents, and immunosuppressants. Despite their potential, many biosynthetic gene clusters (BGCs) in Streptomyces remain silent under standard laboratory conditions. The present study introduces a combination strategy that integrates ribosome engineering and post-translational modification (PTM) to activate the silent BGCs in Streptomyces XH-17, which was identified as S. abikoensis by whole gene cluster sequencing and phylogenetic analysis. The antimicrobial activity of the engineered strain increased by 3.74-fold, 1.40-fold, and 4.08-fold against Alternaria alternata, Fusarium oxysporum, and F. proliferatum, respectively. The main compounds responsible for antifungal activity were identified as α-chaconine and α-solanine by high-resolution mass spectrometry (HRMS), and their BGCs were silent in the wild type (WT). Compared to WT, the two compounds’ production increased by 5.78-fold and 4.68-fold in engineered strain XH-17rpoB+Svp, respectively, and the biosynthetic pathways of α-chaconine and α-solanine were inferred by bioinformatics analysis. This is the first to identify solanine and presumed its biosynthetic pathway from Streptomyces. Our research provides new insights into the control of solanine to protect food safety from Streptomyces contamination. The results from the current investigation provide an effective pipeline to activate silent gene clusters in Streptomyces and offer new insight into discovering new bioactive compounds within this genus.