Engineered biosynthesis and characterization of disaccharide-pimaricin

Abstract Background Disaccharide polyene macrolides exhibit superior water solubility and significantly reduced hemolytic toxicity compared to their monosaccharide counterparts, making them promising candidates for safer antifungal therapeutics. In this study, we engineered a Streptomyces gilvospore...

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Main Authors: Xiaoshan Zuo, Liqin Qiao, Yao Dong, Xing Jin, Zhongyuan Ren, Hao Cui
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Microbial Cell Factories
Subjects:
Online Access:https://doi.org/10.1186/s12934-025-02742-9
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author Xiaoshan Zuo
Liqin Qiao
Yao Dong
Xing Jin
Zhongyuan Ren
Hao Cui
author_facet Xiaoshan Zuo
Liqin Qiao
Yao Dong
Xing Jin
Zhongyuan Ren
Hao Cui
author_sort Xiaoshan Zuo
collection DOAJ
description Abstract Background Disaccharide polyene macrolides exhibit superior water solubility and significantly reduced hemolytic toxicity compared to their monosaccharide counterparts, making them promising candidates for safer antifungal therapeutics. In this study, we engineered a Streptomyces gilvosporeus (pSET152-nppY) capable of producing disaccharide-pimaricin (DSP) through heterologous expression of the nppY gene, which encodes a glycosyltransferase responsible for the second sugar extension in the biosynthetic pathway. Results The novel compound was structurally characterized and designated disaccharide-pimaricin (DSP), featuring an aglycone identical to pimaricin and a unique disaccharide moiety (mycosaminyl-α1–4-N-acetylglucosamine). A purification protocol for DSP was established. Compared to pimaricin, DSP demonstrated a 50% reduction in antifungal activity, a 12.6-fold decrease in hemolytic toxicity, and a remarkable 107.6-fold increase in water solubility. Growth analysis revealed a delayed growth cycle in the mutant strain, suggesting that nppY expression may impose additional metabolic burden. Optimization of the fermentation medium using a statistical design identified an optimal formulation, with a maximum DSP titer of 138.168 mg/L. Conclusions This study underscores the potential of disaccharide polyene macrolides as safer antifungal agents and establishes a robust framework for engineering strains to produce these compounds. The findings provide critical insights into balancing biosynthetic efficiency and strain fitness, advancing the development of next-generation polyene antibiotics.
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spelling doaj-art-72f1867592f14010a485bf520f1c4b462025-08-20T02:29:51ZengBMCMicrobial Cell Factories1475-28592025-05-0124111810.1186/s12934-025-02742-9Engineered biosynthesis and characterization of disaccharide-pimaricinXiaoshan Zuo0Liqin Qiao1Yao Dong2Xing Jin3Zhongyuan Ren4Hao Cui5School of Chemistry and Pharmaceutical Engineering, Jilin Institute of Chemical TechnologySchool of Chemistry and Pharmaceutical Engineering, Jilin Institute of Chemical TechnologyCollege of Biology & Food Engineering, Jilin Institute of Chemical TechnologyDepartment of Anesthesiology, Affiliated Hospital of Beihua University, Jilin Institute of Chemical TechnologyCollege of Biology & Food Engineering, Jilin Institute of Chemical TechnologySchool of Chemistry and Pharmaceutical Engineering, Jilin Institute of Chemical TechnologyAbstract Background Disaccharide polyene macrolides exhibit superior water solubility and significantly reduced hemolytic toxicity compared to their monosaccharide counterparts, making them promising candidates for safer antifungal therapeutics. In this study, we engineered a Streptomyces gilvosporeus (pSET152-nppY) capable of producing disaccharide-pimaricin (DSP) through heterologous expression of the nppY gene, which encodes a glycosyltransferase responsible for the second sugar extension in the biosynthetic pathway. Results The novel compound was structurally characterized and designated disaccharide-pimaricin (DSP), featuring an aglycone identical to pimaricin and a unique disaccharide moiety (mycosaminyl-α1–4-N-acetylglucosamine). A purification protocol for DSP was established. Compared to pimaricin, DSP demonstrated a 50% reduction in antifungal activity, a 12.6-fold decrease in hemolytic toxicity, and a remarkable 107.6-fold increase in water solubility. Growth analysis revealed a delayed growth cycle in the mutant strain, suggesting that nppY expression may impose additional metabolic burden. Optimization of the fermentation medium using a statistical design identified an optimal formulation, with a maximum DSP titer of 138.168 mg/L. Conclusions This study underscores the potential of disaccharide polyene macrolides as safer antifungal agents and establishes a robust framework for engineering strains to produce these compounds. The findings provide critical insights into balancing biosynthetic efficiency and strain fitness, advancing the development of next-generation polyene antibiotics.https://doi.org/10.1186/s12934-025-02742-9Streptomyces gilposporeusGlycosyltransferaseDisaccharide-pimaricinWater-solubleAntifungal activityHemolysis
spellingShingle Xiaoshan Zuo
Liqin Qiao
Yao Dong
Xing Jin
Zhongyuan Ren
Hao Cui
Engineered biosynthesis and characterization of disaccharide-pimaricin
Microbial Cell Factories
Streptomyces gilposporeus
Glycosyltransferase
Disaccharide-pimaricin
Water-soluble
Antifungal activity
Hemolysis
title Engineered biosynthesis and characterization of disaccharide-pimaricin
title_full Engineered biosynthesis and characterization of disaccharide-pimaricin
title_fullStr Engineered biosynthesis and characterization of disaccharide-pimaricin
title_full_unstemmed Engineered biosynthesis and characterization of disaccharide-pimaricin
title_short Engineered biosynthesis and characterization of disaccharide-pimaricin
title_sort engineered biosynthesis and characterization of disaccharide pimaricin
topic Streptomyces gilposporeus
Glycosyltransferase
Disaccharide-pimaricin
Water-soluble
Antifungal activity
Hemolysis
url https://doi.org/10.1186/s12934-025-02742-9
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AT yaodong engineeredbiosynthesisandcharacterizationofdisaccharidepimaricin
AT xingjin engineeredbiosynthesisandcharacterizationofdisaccharidepimaricin
AT zhongyuanren engineeredbiosynthesisandcharacterizationofdisaccharidepimaricin
AT haocui engineeredbiosynthesisandcharacterizationofdisaccharidepimaricin