The Cultivable Bacterial Microbiota Associated to the Medicinal Plant Origanum vulgare L.: From Antibiotic Resistance to Growth-Inhibitory Properties

The insurgence of antibiotic resistance and emergence of multidrug-resistant (MDR) pathogens prioritize research to discover new antimicrobials. In this context, medicinal plants produce bioactive compounds of pharmacological interest: some extracts have antimicrobial properties that can contrast di...

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Main Authors: Lara Mitia Castronovo, Carmela Calonico, Roberta Ascrizzi, Sara Del Duca, Vania Delfino, Sofia Chioccioli, Alberto Vassallo, Iolanda Strozza, Marinella De Leo, Sauro Biffi, Giovanni Bacci, Patrizia Bogani, Valentina Maggini, Alessio Mengoni, Luisa Pistelli, Antonella Lo Nostro, Fabio Firenzuoli, Renato Fani
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.00862/full
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author Lara Mitia Castronovo
Carmela Calonico
Roberta Ascrizzi
Sara Del Duca
Vania Delfino
Sofia Chioccioli
Alberto Vassallo
Iolanda Strozza
Marinella De Leo
Sauro Biffi
Giovanni Bacci
Patrizia Bogani
Valentina Maggini
Valentina Maggini
Alessio Mengoni
Luisa Pistelli
Antonella Lo Nostro
Fabio Firenzuoli
Renato Fani
spellingShingle Lara Mitia Castronovo
Carmela Calonico
Roberta Ascrizzi
Sara Del Duca
Vania Delfino
Sofia Chioccioli
Alberto Vassallo
Iolanda Strozza
Marinella De Leo
Sauro Biffi
Giovanni Bacci
Patrizia Bogani
Valentina Maggini
Valentina Maggini
Alessio Mengoni
Luisa Pistelli
Antonella Lo Nostro
Fabio Firenzuoli
Renato Fani
The Cultivable Bacterial Microbiota Associated to the Medicinal Plant Origanum vulgare L.: From Antibiotic Resistance to Growth-Inhibitory Properties
Frontiers in Microbiology
antimicrobial compounds
medicinal plants
Origanum vulgare
endophytic bacteria
antibiotic resistance
author_facet Lara Mitia Castronovo
Carmela Calonico
Roberta Ascrizzi
Sara Del Duca
Vania Delfino
Sofia Chioccioli
Alberto Vassallo
Iolanda Strozza
Marinella De Leo
Sauro Biffi
Giovanni Bacci
Patrizia Bogani
Valentina Maggini
Valentina Maggini
Alessio Mengoni
Luisa Pistelli
Antonella Lo Nostro
Fabio Firenzuoli
Renato Fani
author_sort Lara Mitia Castronovo
title The Cultivable Bacterial Microbiota Associated to the Medicinal Plant Origanum vulgare L.: From Antibiotic Resistance to Growth-Inhibitory Properties
title_short The Cultivable Bacterial Microbiota Associated to the Medicinal Plant Origanum vulgare L.: From Antibiotic Resistance to Growth-Inhibitory Properties
title_full The Cultivable Bacterial Microbiota Associated to the Medicinal Plant Origanum vulgare L.: From Antibiotic Resistance to Growth-Inhibitory Properties
title_fullStr The Cultivable Bacterial Microbiota Associated to the Medicinal Plant Origanum vulgare L.: From Antibiotic Resistance to Growth-Inhibitory Properties
title_full_unstemmed The Cultivable Bacterial Microbiota Associated to the Medicinal Plant Origanum vulgare L.: From Antibiotic Resistance to Growth-Inhibitory Properties
title_sort cultivable bacterial microbiota associated to the medicinal plant origanum vulgare l.: from antibiotic resistance to growth-inhibitory properties
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-05-01
description The insurgence of antibiotic resistance and emergence of multidrug-resistant (MDR) pathogens prioritize research to discover new antimicrobials. In this context, medicinal plants produce bioactive compounds of pharmacological interest: some extracts have antimicrobial properties that can contrast different pathogens. For such a purpose, Origanum vulgare L. (Lamiaceae family) is a medicinal aromatic plant, whose essential oil (EO) is recognized for its antiseptic, antimicrobial and antiviral activities. The cultivable bacteria from different compartments (i.e., flower, leaf, stem and soil) were isolated in order to: (i) characterize the bacterial microbiota associated to the plant, determining the forces responsible for the structuring of its composition (by evaluation of cross inhibition); (ii) investigate if bacterial endophytes demonstrate antimicrobial activities against human pathogens. A pool of plants belonging to O. vulgare species was collected and the specimen chemotype was defined by hydrodistillation of its essential oil. The isolation of plant associated bacteria was performed from the four compartments. Microbiota was further characterized through a culture-independent approach and next-generation sequencing analysis, as well. Isolates were molecularly typed by Random Amplified Polymorphic DNA (RAPD) profiling and taxonomically assigned by 16S rRNA gene sequencing. Antibiotic resistance profiles of isolates and pairwise cross-inhibition of isolates on agar plates (i.e., antagonistic interactions) were also assessed. High level of diversity of bacterial isolates was detected at both genus and strain level in all different compartments. Most strains were tolerant against common antibiotics; moreover, they produced antagonistic patterns of interactions mainly with strains from different compartments with respect to that of original isolation. Strains that exhibited high inhibitory properties were further tested against human pathogens, revealing a strong capacity to inhibit the growth of strains resistant to several antibiotics. In conclusion, this study regarded the characterization of O. vulgare L. chemotype and of the bacterial communities associated to this medicinal plant, also allowing the evaluation of antibiotic resistance and antagonistic interactions. This study provided the bases for further analyses on the possible involvement of endophytic bacteria in the production of antimicrobial molecules that could have an important role in clinical and therapeutic applications.
topic antimicrobial compounds
medicinal plants
Origanum vulgare
endophytic bacteria
antibiotic resistance
url https://www.frontiersin.org/article/10.3389/fmicb.2020.00862/full
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spelling doaj-e1c74d3f314540a88f1bef95d9f8a6f82020-11-25T02:07:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-05-011110.3389/fmicb.2020.00862535811The Cultivable Bacterial Microbiota Associated to the Medicinal Plant Origanum vulgare L.: From Antibiotic Resistance to Growth-Inhibitory PropertiesLara Mitia Castronovo0Carmela Calonico1Roberta Ascrizzi2Sara Del Duca3Vania Delfino4Sofia Chioccioli5Alberto Vassallo6Iolanda Strozza7Marinella De Leo8Sauro Biffi9Giovanni Bacci10Patrizia Bogani11Valentina Maggini12Valentina Maggini13Alessio Mengoni14Luisa Pistelli15Antonella Lo Nostro16Fabio Firenzuoli17Renato Fani18Department of Biology, University of Florence, Sesto Fiorentino, ItalyDepartment of Health Sciences, University of Florence, Florence, ItalyDepartment of Pharmacy, University of Pisa, Pisa, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyDepartment of Health Sciences, University of Florence, Florence, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyDepartment of Pharmacy, University of Pisa, Pisa, ItalyGiardino delle Erbe, Casola Valsenio, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyResearch and Innovation Center in Phytotherapy and Integrated Medicine – CERFIT Careggi University Hospital, Florence, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyDepartment of Pharmacy, University of Pisa, Pisa, ItalyDepartment of Health Sciences, University of Florence, Florence, ItalyResearch and Innovation Center in Phytotherapy and Integrated Medicine – CERFIT Careggi University Hospital, Florence, ItalyDepartment of Biology, University of Florence, Sesto Fiorentino, ItalyThe insurgence of antibiotic resistance and emergence of multidrug-resistant (MDR) pathogens prioritize research to discover new antimicrobials. In this context, medicinal plants produce bioactive compounds of pharmacological interest: some extracts have antimicrobial properties that can contrast different pathogens. For such a purpose, Origanum vulgare L. (Lamiaceae family) is a medicinal aromatic plant, whose essential oil (EO) is recognized for its antiseptic, antimicrobial and antiviral activities. The cultivable bacteria from different compartments (i.e., flower, leaf, stem and soil) were isolated in order to: (i) characterize the bacterial microbiota associated to the plant, determining the forces responsible for the structuring of its composition (by evaluation of cross inhibition); (ii) investigate if bacterial endophytes demonstrate antimicrobial activities against human pathogens. A pool of plants belonging to O. vulgare species was collected and the specimen chemotype was defined by hydrodistillation of its essential oil. The isolation of plant associated bacteria was performed from the four compartments. Microbiota was further characterized through a culture-independent approach and next-generation sequencing analysis, as well. Isolates were molecularly typed by Random Amplified Polymorphic DNA (RAPD) profiling and taxonomically assigned by 16S rRNA gene sequencing. Antibiotic resistance profiles of isolates and pairwise cross-inhibition of isolates on agar plates (i.e., antagonistic interactions) were also assessed. High level of diversity of bacterial isolates was detected at both genus and strain level in all different compartments. Most strains were tolerant against common antibiotics; moreover, they produced antagonistic patterns of interactions mainly with strains from different compartments with respect to that of original isolation. Strains that exhibited high inhibitory properties were further tested against human pathogens, revealing a strong capacity to inhibit the growth of strains resistant to several antibiotics. In conclusion, this study regarded the characterization of O. vulgare L. chemotype and of the bacterial communities associated to this medicinal plant, also allowing the evaluation of antibiotic resistance and antagonistic interactions. This study provided the bases for further analyses on the possible involvement of endophytic bacteria in the production of antimicrobial molecules that could have an important role in clinical and therapeutic applications.https://www.frontiersin.org/article/10.3389/fmicb.2020.00862/fullantimicrobial compoundsmedicinal plantsOriganum vulgareendophytic bacteriaantibiotic resistance