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Antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant Corynebacterium striatum

BACKGROUND: Corynebacterium striatum is a microorganism with an excellent capacity for biofilm production and thus has been correlated with nosocomial transmission and invasive infections. However, little is known about the mechanism of biofilm formation of this commensal pathogen. In this study, we...

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Autores principales: Wen, Juan, Wang, Zhaohui, Du, Xiaoli, Liu, Roushan, Wang, Junrui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9700914/
https://www.ncbi.nlm.nih.gov/pubmed/36434697
http://dx.doi.org/10.1186/s12941-022-00546-y
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author Wen, Juan
Wang, Zhaohui
Du, Xiaoli
Liu, Roushan
Wang, Junrui
author_facet Wen, Juan
Wang, Zhaohui
Du, Xiaoli
Liu, Roushan
Wang, Junrui
author_sort Wen, Juan
collection PubMed
description BACKGROUND: Corynebacterium striatum is a microorganism with an excellent capacity for biofilm production and thus has been correlated with nosocomial transmission and invasive infections. However, little is known about the mechanism of biofilm formation of this commensal pathogen. In this study, we aimed to investigate the biofilm formation abilities of multidrug-resistant Corynebacterium striatum clinical isolates and the roles of extracellular proteins, exopolysaccharides and extracellular DNA in mediating more robust biofilm formation by the isolates of C. striatum. METHODS: C. striatum isolates were identified using VITEK-2 ANC card, matrix-assisted laser desorption/ionization-time of flight mass spectrometry and 16S rRNA sequencing. The antibiotic susceptibility test was performed using the broth microdilution method. The distribution of spaDEF genes among C. striatum isolates was detected by polymerase chain reaction, and pulsed-field gel electrophoresis typing was employed to analyze the genotypes of the isolates. Crystal violet staining and scanning electron microscopy techniques were used to detect biofilm production by C. striatum isolates. Biofilm degradation assay was performed to observe the effects of extracellular matrix degradative agents (proteinase K, dispersin B, and DNase I) on C. striatum biofilms. RESULTS: Twenty-seven C. striatum isolates were enrolled in the study, and the resistance rates were the highest (100%, 27/27) against penicillin and ceftriaxone. Approximately 96.3% (26/27) C. striatum isolates were resistant to at least three different types of antimicrobial agents tested. All isolates were confirmed to be biofilm producers, and 74.07% (20/27) isolates presented moderate to strong biofilm production abilities. P7 genotype (44.4%, 12/27) was identified to as the predominant genotype, and all of isolates belonging to this genotype were multidrug-resistant and had stronger biofilm-forming abilities. Most C. striatum isolates (74.07%, 20/27) carry spaD, spaE, and spaF genes, which encode spa-type pili. However, the correlation between the expression of spa-type genes and the biofilm production abilities of the C. striatum isolates was not found. The biofilms of 80% (8/10), 90% (9/10), and 100% (10/10) C. striatum isolates with moderate to strong biofilm production abilities were significantly eliminated upon the treatment of dispersin B (20 μg/mL), DNase I (20 μg/mL), and proteinase K (20 μg/mL) (p < 0.05), respectively. For the combination groups with two kinds of biofilm-degradative agents, the combination of 20 μg/mL proteinase K/dispersin B showed the strongest biofilm-eliminating effects, when the biofilms of 90% (9/10) C. striatum isolates degraded more than 50%. CONCLUSIONS: The C. striatum isolates that belonged to the predominant genotype showed a multidrug resistance (MDR) phenotype and strong biofilm formation abilities. Extracellular matrix seems to be an essential determinant in mediating biofilm formation of MDR C. striatum, since extracellular matrix degradative agents (proteinase K, dispersin B and DNase I) showed strong biofilm-eliminating effects toward multidrug-resistant C. striatum isolates. The findings of this study highlight new ideas/directions to explore the whole nature of biofilm formation of C. striatum and the function of extracellular matrix in this process. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12941-022-00546-y.
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spelling pubmed-97009142022-11-27 Antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant Corynebacterium striatum Wen, Juan Wang, Zhaohui Du, Xiaoli Liu, Roushan Wang, Junrui Ann Clin Microbiol Antimicrob Research BACKGROUND: Corynebacterium striatum is a microorganism with an excellent capacity for biofilm production and thus has been correlated with nosocomial transmission and invasive infections. However, little is known about the mechanism of biofilm formation of this commensal pathogen. In this study, we aimed to investigate the biofilm formation abilities of multidrug-resistant Corynebacterium striatum clinical isolates and the roles of extracellular proteins, exopolysaccharides and extracellular DNA in mediating more robust biofilm formation by the isolates of C. striatum. METHODS: C. striatum isolates were identified using VITEK-2 ANC card, matrix-assisted laser desorption/ionization-time of flight mass spectrometry and 16S rRNA sequencing. The antibiotic susceptibility test was performed using the broth microdilution method. The distribution of spaDEF genes among C. striatum isolates was detected by polymerase chain reaction, and pulsed-field gel electrophoresis typing was employed to analyze the genotypes of the isolates. Crystal violet staining and scanning electron microscopy techniques were used to detect biofilm production by C. striatum isolates. Biofilm degradation assay was performed to observe the effects of extracellular matrix degradative agents (proteinase K, dispersin B, and DNase I) on C. striatum biofilms. RESULTS: Twenty-seven C. striatum isolates were enrolled in the study, and the resistance rates were the highest (100%, 27/27) against penicillin and ceftriaxone. Approximately 96.3% (26/27) C. striatum isolates were resistant to at least three different types of antimicrobial agents tested. All isolates were confirmed to be biofilm producers, and 74.07% (20/27) isolates presented moderate to strong biofilm production abilities. P7 genotype (44.4%, 12/27) was identified to as the predominant genotype, and all of isolates belonging to this genotype were multidrug-resistant and had stronger biofilm-forming abilities. Most C. striatum isolates (74.07%, 20/27) carry spaD, spaE, and spaF genes, which encode spa-type pili. However, the correlation between the expression of spa-type genes and the biofilm production abilities of the C. striatum isolates was not found. The biofilms of 80% (8/10), 90% (9/10), and 100% (10/10) C. striatum isolates with moderate to strong biofilm production abilities were significantly eliminated upon the treatment of dispersin B (20 μg/mL), DNase I (20 μg/mL), and proteinase K (20 μg/mL) (p < 0.05), respectively. For the combination groups with two kinds of biofilm-degradative agents, the combination of 20 μg/mL proteinase K/dispersin B showed the strongest biofilm-eliminating effects, when the biofilms of 90% (9/10) C. striatum isolates degraded more than 50%. CONCLUSIONS: The C. striatum isolates that belonged to the predominant genotype showed a multidrug resistance (MDR) phenotype and strong biofilm formation abilities. Extracellular matrix seems to be an essential determinant in mediating biofilm formation of MDR C. striatum, since extracellular matrix degradative agents (proteinase K, dispersin B and DNase I) showed strong biofilm-eliminating effects toward multidrug-resistant C. striatum isolates. The findings of this study highlight new ideas/directions to explore the whole nature of biofilm formation of C. striatum and the function of extracellular matrix in this process. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12941-022-00546-y. BioMed Central 2022-11-25 /pmc/articles/PMC9700914/ /pubmed/36434697 http://dx.doi.org/10.1186/s12941-022-00546-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wen, Juan
Wang, Zhaohui
Du, Xiaoli
Liu, Roushan
Wang, Junrui
Antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant Corynebacterium striatum
title Antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant Corynebacterium striatum
title_full Antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant Corynebacterium striatum
title_fullStr Antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant Corynebacterium striatum
title_full_unstemmed Antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant Corynebacterium striatum
title_short Antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant Corynebacterium striatum
title_sort antibioflm effects of extracellular matrix degradative agents on the biofilm of different strains of multi-drug resistant corynebacterium striatum
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9700914/
https://www.ncbi.nlm.nih.gov/pubmed/36434697
http://dx.doi.org/10.1186/s12941-022-00546-y
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