From Function to Metabolome: Metabolomic Analysis Reveals the Effect of Probiotic Fermentation on the Chemical Compositions and Biological Activities of Perilla frutescens Leaves

Zhenxing Wang; Ximeng Jin; Xuechun Zhang; Xing Xie; Zongcai Tu; Xiahong He

doi:10.3389/fnut.2022.933193

From Function to Metabolome: Metabolomic Analysis Reveals the Effect of Probiotic Fermentation on the Chemical Compositions and Biological Activities of Perilla frutescens Leaves

Front Nutr. 2022 Jul 11:9:933193. doi: 10.3389/fnut.2022.933193. eCollection 2022.

Authors

Zhenxing Wang^{1

2

3}, Ximeng Jin², Xuechun Zhang², Xing Xie³, Zongcai Tu³, Xiahong He^{1

4}

Affiliations

¹ Key Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Ministry of Education, Southwest Forestry University, Kunming, China.
² College of Life Sciences, Southwest Forestry University, Kunming, China.
³ National R&D Center for Freshwater Fish Processing, College of Health, Jiangxi Normal University, Nanchang, China.
⁴ College of Horticulture and Landscape, Southwest Forestry University, Kunming, China.

Abstract

This study aimed to investigate the impact of probiotic fermentation on the active components and functions of Perilla frutescens leaves (PFL). PFL was fermented for 7 days using six probiotics (Lactobacillus Plantarum SWFU D16, Lactobacillus Plantarum ATCC 8014, Lactobacillus Rhamnosus ATCC 53013, Streptococcus Thermophilus CICC 6038, Lactobacillus Casei ATCC 334, and Lactobacillus Bulgaricus CICC 6045). The total phenol and flavonoid contents, antioxidant abilities, as well as α-glucosidase and acetylcholinesterase inhibition abilities of PFL during the fermentation process were evaluated, and its bioactive compounds were further quantified by high-performance liquid chromatography (HPLC). Finally, non-targeted ultra-HPLC-tandem mass spectroscopy was used to identify the metabolites affected by fermentation and explore the possible mechanisms of the action of fermentation. The results showed that most of the active component contents and functional activities of PFL exhibited that it first increased and then decreased, and different probiotics had clearly distinguishable effects from each other, of which fermentation with ATCC 53013 for 1 day showed the highest enhancement effect. The same trend was also confirmed by the result of the changes in the contents of 12 phenolic acids and flavonoids by HPLC analysis. Further metabolomic analysis revealed significant metabolite changes under the best fermentation condition, which involved primarily the generation of fatty acids and their conjugates, flavonoids. A total of 574 and 387 metabolites were identified in positive ion and negative ion modes, respectively. Results of Spearman's analysis indicated that some primary metabolites and secondary metabolites such as flavonoids, phenols, and fatty acids might play an important role in the functional activity of PFL. Differential metabolites were subjected to the KEGG database and 97 metabolites pathways were obtained, of which biosyntheses of unsaturated fatty acids, flavonoid, and isoflavonoid were the most enriched pathways. The above results revealed the potential reason for the differences in metabolic and functional levels of PFL after fermentation. This study could provide a scientific basis for the further study of PFL, as well as novel insights into the action mechanism of probiotic fermentation on the chemical composition and biological activity of food/drug.

Keywords: Perilla frutescens leaves; biological activity; fermentation; metabolomics; phytochemical composition.

Grants and funding

This work was supported by Yunnan Agricultural Joint Special General Project (202101BD070001-109 and 202101BD070001-089), China Agriculture Research System (CARS-21), Yunnan Special General Projects of Basic Research (202201AT070049), Major Science and Technology Project of Yunnan and Kunming (202102AE090042 and 2019ZG0901), Scientific Research Fund Project of Yunnan Provincial Department of Education (2022J0507), and Major Science and Technology Project of Kunming (2021JH002).