Gene expression dynamics in Bacillus cereus and Bacillus subtilis treated with Thymus vulgaris and Origanum vulgare subsp. hirtum essential oils

Essential oils (EOs) hold significant potential as antimicrobials in food, due to their high concentration of active phenolic compounds. These compounds can target bacterial cells through various mechanisms, such as membrane disruption, quorum sensing inhibition, and interference in virulence factor...

Full description

Saved in:
Bibliographic Details
Main Authors: Fabrizio Anniballi, Chiara Purgatorio, Annalisa Serio, Concetta Scalfaro, Silvia Taglieri, Antonello Paparella
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1643608/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849229168358719488
author Fabrizio Anniballi
Chiara Purgatorio
Annalisa Serio
Concetta Scalfaro
Silvia Taglieri
Antonello Paparella
author_facet Fabrizio Anniballi
Chiara Purgatorio
Annalisa Serio
Concetta Scalfaro
Silvia Taglieri
Antonello Paparella
author_sort Fabrizio Anniballi
collection DOAJ
description Essential oils (EOs) hold significant potential as antimicrobials in food, due to their high concentration of active phenolic compounds. These compounds can target bacterial cells through various mechanisms, such as membrane disruption, quorum sensing inhibition, and interference in virulence factors, affecting microorganisms at a genomic level. Bacillus cereus and Bacillus subtilis are key foodborne bacteria that could be managed using these natural preservatives. The present study investigated the effects of stress induced by applying Thymus vulgaris and Origanum vulgare subsp. hirtum EOs on genetic modifications in B. cereus 11 and B. subtilis 58C strains isolated from shelf-stable gnocchi, through their gene expression analysis by quantitative real-time RT-PCR. Sublethal EO concentrations were tested, at increasing time intervals (6, 12, 18, 24, and 48 h). Most of the genes were downregulated at 6 h, indicating that the stressful situation prolonged the lag phase. Only spo0A for both B. cereus and B. subtilis, and pbpF and sigB for B. subtilis were upregulated after 6 h, suggesting an attempt to restore cellular communication and repair membrane damage. The pbpF gene was the most significant in the stress response of B. subtilis. Conversely, B. cereus responded through different mechanisms, primarily driven by the plcR and nheB genes, illustrating the role of virulence mechanisms in its stress response. In both strains, the genes were generally more upregulated at a higher concentration of EO (0.58 mg/mL), which was more stimulating than at 0.29 mg/mL. Moreover, the two EOs elicited variable stress responses, which implies different cellular mechanisms and genes in the same microorganism. Therefore, the outcomes of this study suggest that the action of the two EOs mainly influenced cell membrane integrity and quorum sensing mechanisms, with differences in the genes involved for the two species and the two EOs.
format Article
id doaj-art-71b6cb55c36b44c4ba5b899ba9cb0efc
institution Kabale University
issn 1664-302X
language English
publishDate 2025-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj-art-71b6cb55c36b44c4ba5b899ba9cb0efc2025-08-22T05:26:58ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-08-011610.3389/fmicb.2025.16436081643608Gene expression dynamics in Bacillus cereus and Bacillus subtilis treated with Thymus vulgaris and Origanum vulgare subsp. hirtum essential oilsFabrizio Anniballi0Chiara Purgatorio1Annalisa Serio2Concetta Scalfaro3Silvia Taglieri4Antonello Paparella5National Reference Centre for Botulism, Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Rome, ItalyDepartment of Bioscience and Technology for Food, Agriculture and Environment, University of Teramo, Teramo, ItalyDepartment of Bioscience and Technology for Food, Agriculture and Environment, University of Teramo, Teramo, ItalyNational Reference Centre for Botulism, Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Rome, ItalyNational Reference Centre for Botulism, Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Rome, ItalyDepartment of Bioscience and Technology for Food, Agriculture and Environment, University of Teramo, Teramo, ItalyEssential oils (EOs) hold significant potential as antimicrobials in food, due to their high concentration of active phenolic compounds. These compounds can target bacterial cells through various mechanisms, such as membrane disruption, quorum sensing inhibition, and interference in virulence factors, affecting microorganisms at a genomic level. Bacillus cereus and Bacillus subtilis are key foodborne bacteria that could be managed using these natural preservatives. The present study investigated the effects of stress induced by applying Thymus vulgaris and Origanum vulgare subsp. hirtum EOs on genetic modifications in B. cereus 11 and B. subtilis 58C strains isolated from shelf-stable gnocchi, through their gene expression analysis by quantitative real-time RT-PCR. Sublethal EO concentrations were tested, at increasing time intervals (6, 12, 18, 24, and 48 h). Most of the genes were downregulated at 6 h, indicating that the stressful situation prolonged the lag phase. Only spo0A for both B. cereus and B. subtilis, and pbpF and sigB for B. subtilis were upregulated after 6 h, suggesting an attempt to restore cellular communication and repair membrane damage. The pbpF gene was the most significant in the stress response of B. subtilis. Conversely, B. cereus responded through different mechanisms, primarily driven by the plcR and nheB genes, illustrating the role of virulence mechanisms in its stress response. In both strains, the genes were generally more upregulated at a higher concentration of EO (0.58 mg/mL), which was more stimulating than at 0.29 mg/mL. Moreover, the two EOs elicited variable stress responses, which implies different cellular mechanisms and genes in the same microorganism. Therefore, the outcomes of this study suggest that the action of the two EOs mainly influenced cell membrane integrity and quorum sensing mechanisms, with differences in the genes involved for the two species and the two EOs.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1643608/fullBacillus cereusBacillus subtilisThymus vulgarisOriganum vulgare subsp. hirtumessential oilsgene expression Bacillus cereus
spellingShingle Fabrizio Anniballi
Chiara Purgatorio
Annalisa Serio
Concetta Scalfaro
Silvia Taglieri
Antonello Paparella
Gene expression dynamics in Bacillus cereus and Bacillus subtilis treated with Thymus vulgaris and Origanum vulgare subsp. hirtum essential oils
Frontiers in Microbiology
Bacillus cereus
Bacillus subtilis
Thymus vulgaris
Origanum vulgare subsp. hirtum
essential oils
gene expression Bacillus cereus
title Gene expression dynamics in Bacillus cereus and Bacillus subtilis treated with Thymus vulgaris and Origanum vulgare subsp. hirtum essential oils
title_full Gene expression dynamics in Bacillus cereus and Bacillus subtilis treated with Thymus vulgaris and Origanum vulgare subsp. hirtum essential oils
title_fullStr Gene expression dynamics in Bacillus cereus and Bacillus subtilis treated with Thymus vulgaris and Origanum vulgare subsp. hirtum essential oils
title_full_unstemmed Gene expression dynamics in Bacillus cereus and Bacillus subtilis treated with Thymus vulgaris and Origanum vulgare subsp. hirtum essential oils
title_short Gene expression dynamics in Bacillus cereus and Bacillus subtilis treated with Thymus vulgaris and Origanum vulgare subsp. hirtum essential oils
title_sort gene expression dynamics in bacillus cereus and bacillus subtilis treated with thymus vulgaris and origanum vulgare subsp hirtum essential oils
topic Bacillus cereus
Bacillus subtilis
Thymus vulgaris
Origanum vulgare subsp. hirtum
essential oils
gene expression Bacillus cereus
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1643608/full
work_keys_str_mv AT fabrizioanniballi geneexpressiondynamicsinbacilluscereusandbacillussubtilistreatedwiththymusvulgarisandoriganumvulgaresubsphirtumessentialoils
AT chiarapurgatorio geneexpressiondynamicsinbacilluscereusandbacillussubtilistreatedwiththymusvulgarisandoriganumvulgaresubsphirtumessentialoils
AT annalisaserio geneexpressiondynamicsinbacilluscereusandbacillussubtilistreatedwiththymusvulgarisandoriganumvulgaresubsphirtumessentialoils
AT concettascalfaro geneexpressiondynamicsinbacilluscereusandbacillussubtilistreatedwiththymusvulgarisandoriganumvulgaresubsphirtumessentialoils
AT silviataglieri geneexpressiondynamicsinbacilluscereusandbacillussubtilistreatedwiththymusvulgarisandoriganumvulgaresubsphirtumessentialoils
AT antonellopaparella geneexpressiondynamicsinbacilluscereusandbacillussubtilistreatedwiththymusvulgarisandoriganumvulgaresubsphirtumessentialoils