Exploration of Antibacterial Compounds From Bacillus velezensis BP1 Against Foodborne Pathogens Staphylococcus aureus and Salmonella enterica Typhimurium Using Metabolomic and Genomic Approaches
IF 2.1 4区 农林科学Q3 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
Tsania Taskia Nabila , Ema Damayanti , Jaka Widada
{"title":"Exploration of Antibacterial Compounds From Bacillus velezensis BP1 Against Foodborne Pathogens Staphylococcus aureus and Salmonella enterica Typhimurium Using Metabolomic and Genomic Approaches","authors":"Tsania Taskia Nabila , Ema Damayanti , Jaka Widada","doi":"10.1016/j.jfp.2025.100546","DOIUrl":null,"url":null,"abstract":"<div><div>Food contamination by pathogenic microorganisms has become a significant issue. This study investigated the antibacterial compounds of a <em>Bacillus</em> isolate from stingless bee bread, <em>Bacillus velezensis</em> BP1, against foodborne pathogens <em>Staphylococcus aureus</em> ATCC 25923 and <em>Salmonella enterica</em> Typhimurium ATCC 14028 using the one strain many compounds (OSMAC), metabolomic, and genomic approaches. The culture media used were Tryptic Soy Broth (TSB), TSB with Chitosan (TSB-Chi), several synthetic broths composed of Mineral Salts with Glucose (MG) and Glucose-Fructose (MGF), Carboxymethyl Cellulose (CMC), and Starch Nitrate (SNB), to analyze diverse antibacterial compounds. Twelve extracts from the supernatant (S) and pellet (P) were screened using the microdilution method. P-TSB and S-TSB-Chi demonstrated the highest antibacterial effects, with inhibitory concentration (IC<sub>50</sub>) values of 253.5 ppm and 740.28 ppm, respectively. Fourier transform infrared spectroscopy (FTIR) analysis identified an amide I group contributing to extract clustering. Untargeted liquid chromatography-high resolution mass spectrometry (LC-HRMS) revealed six compounds significantly contributing to extract clustering. Enrichment analysis showed that chitosan was associated with the metabolic processes of pyrimidine and nucleotide metabolisms. Growth curve assay and scanning electron microscopy (SEM) confirmed the extracts’ efficacy. The <em>Bacillus</em> isolate showed an average nucleotide identity (ANI) of 98.08% to <em>Bacillus velezensis</em> NRRL B-41580. Genome mining revealed twelve biosynthetic gene clusters, six 100% similar to known clusters. Molecular docking demonstrated that genome mining-derived bacillibactin and LC-HRMS-derived bis(4-ethylbenzylidene)sorbitol and cyclo(phenylalanyl-prolyl) exhibited the strongest binding affinities against four pathogen-associated proteins, outperforming ampicillin. This study highlights <em>Bacillus velezensis</em> BP1’s potential as a source of diverse antibacterial compounds.</div></div>","PeriodicalId":15903,"journal":{"name":"Journal of food protection","volume":"88 7","pages":"Article 100546"},"PeriodicalIF":2.1000,"publicationDate":"2025-05-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of food protection","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0362028X25000985","RegionNum":4,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Food contamination by pathogenic microorganisms has become a significant issue. This study investigated the antibacterial compounds of a Bacillus isolate from stingless bee bread, Bacillus velezensis BP1, against foodborne pathogens Staphylococcus aureus ATCC 25923 and Salmonella enterica Typhimurium ATCC 14028 using the one strain many compounds (OSMAC), metabolomic, and genomic approaches. The culture media used were Tryptic Soy Broth (TSB), TSB with Chitosan (TSB-Chi), several synthetic broths composed of Mineral Salts with Glucose (MG) and Glucose-Fructose (MGF), Carboxymethyl Cellulose (CMC), and Starch Nitrate (SNB), to analyze diverse antibacterial compounds. Twelve extracts from the supernatant (S) and pellet (P) were screened using the microdilution method. P-TSB and S-TSB-Chi demonstrated the highest antibacterial effects, with inhibitory concentration (IC50) values of 253.5 ppm and 740.28 ppm, respectively. Fourier transform infrared spectroscopy (FTIR) analysis identified an amide I group contributing to extract clustering. Untargeted liquid chromatography-high resolution mass spectrometry (LC-HRMS) revealed six compounds significantly contributing to extract clustering. Enrichment analysis showed that chitosan was associated with the metabolic processes of pyrimidine and nucleotide metabolisms. Growth curve assay and scanning electron microscopy (SEM) confirmed the extracts’ efficacy. The Bacillus isolate showed an average nucleotide identity (ANI) of 98.08% to Bacillus velezensis NRRL B-41580. Genome mining revealed twelve biosynthetic gene clusters, six 100% similar to known clusters. Molecular docking demonstrated that genome mining-derived bacillibactin and LC-HRMS-derived bis(4-ethylbenzylidene)sorbitol and cyclo(phenylalanyl-prolyl) exhibited the strongest binding affinities against four pathogen-associated proteins, outperforming ampicillin. This study highlights Bacillus velezensis BP1’s potential as a source of diverse antibacterial compounds.
期刊介绍:
The Journal of Food Protection® (JFP) is an international, monthly scientific journal in the English language published by the International Association for Food Protection (IAFP). JFP publishes research and review articles on all aspects of food protection and safety. Major emphases of JFP are placed on studies dealing with:
Tracking, detecting (including traditional, molecular, and real-time), inactivating, and controlling food-related hazards, including microorganisms (including antibiotic resistance), microbial (mycotoxins, seafood toxins) and non-microbial toxins (heavy metals, pesticides, veterinary drug residues, migrants from food packaging, and processing contaminants), allergens and pests (insects, rodents) in human food, pet food and animal feed throughout the food chain;
Microbiological food quality and traditional/novel methods to assay microbiological food quality;
Prevention of food-related hazards and food spoilage through food preservatives and thermal/non-thermal processes, including process validation;
Food fermentations and food-related probiotics;
Safe food handling practices during pre-harvest, harvest, post-harvest, distribution and consumption, including food safety education for retailers, foodservice, and consumers;
Risk assessments for food-related hazards;
Economic impact of food-related hazards, foodborne illness, food loss, food spoilage, and adulterated foods;
Food fraud, food authentication, food defense, and foodborne disease outbreak investigations.