Cargando…

A Synthetic Polymicrobial Community Biofilm Model Demonstrates Spatial Partitioning, Tolerance to Antimicrobial Treatment, Reduced Metabolism, and Small Colony Variants Typical of Chronic Wound Biofilms

Understanding chronic wound infection is key for successful treatment and requires accurate laboratory models. We describe a modified biofilm flow device that effectively mimics the chronic wound environment, including simulated wound fluid, a collagen-based 3D biofilm matrix, and a five-species mix...

Descripción completa

Detalles Bibliográficos
Autores principales: Khalid, Ammara, Cookson, Alan R., Whitworth, David E., Beeton, Michael L., Robins, Lori I., Maddocks, Sarah E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9862141/
https://www.ncbi.nlm.nih.gov/pubmed/36678466
http://dx.doi.org/10.3390/pathogens12010118
_version_ 1784875019164188672
author Khalid, Ammara
Cookson, Alan R.
Whitworth, David E.
Beeton, Michael L.
Robins, Lori I.
Maddocks, Sarah E.
author_facet Khalid, Ammara
Cookson, Alan R.
Whitworth, David E.
Beeton, Michael L.
Robins, Lori I.
Maddocks, Sarah E.
author_sort Khalid, Ammara
collection PubMed
description Understanding chronic wound infection is key for successful treatment and requires accurate laboratory models. We describe a modified biofilm flow device that effectively mimics the chronic wound environment, including simulated wound fluid, a collagen-based 3D biofilm matrix, and a five-species mixture of clinically relevant bacteria (Pseudomonas aeruginosa, Staphylococcus aureus, Escherichia coli, Enterococcus faecalis, and Citrobacter freundii). Mixed biofilms were cultured for between 3 and 14 days with consistent numbers of bacteria that exhibited reduced metabolic activity, which increased with a high dose of glucose. S. aureus was recovered from biofilms as a small colony variant, but as a normal colony variant if P. aeruginosa was excluded from the system. Bacteria within the biofilm did not co-aggregate but formed discrete, species-specific clusters. Biofilms demonstrated differential tolerance to the topical antimicrobials Neosporin and HOCl, consistent with protection due to the biofilm lifestyle. The characteristics exhibited within this model match those of real-world wound biofilms, reflecting the clinical scenario and yielding a powerful in vitro tool that is versatile, inexpensive, and pivotal for understanding chronic wound infection.
format Online
Article
Text
id pubmed-9862141
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-98621412023-01-22 A Synthetic Polymicrobial Community Biofilm Model Demonstrates Spatial Partitioning, Tolerance to Antimicrobial Treatment, Reduced Metabolism, and Small Colony Variants Typical of Chronic Wound Biofilms Khalid, Ammara Cookson, Alan R. Whitworth, David E. Beeton, Michael L. Robins, Lori I. Maddocks, Sarah E. Pathogens Article Understanding chronic wound infection is key for successful treatment and requires accurate laboratory models. We describe a modified biofilm flow device that effectively mimics the chronic wound environment, including simulated wound fluid, a collagen-based 3D biofilm matrix, and a five-species mixture of clinically relevant bacteria (Pseudomonas aeruginosa, Staphylococcus aureus, Escherichia coli, Enterococcus faecalis, and Citrobacter freundii). Mixed biofilms were cultured for between 3 and 14 days with consistent numbers of bacteria that exhibited reduced metabolic activity, which increased with a high dose of glucose. S. aureus was recovered from biofilms as a small colony variant, but as a normal colony variant if P. aeruginosa was excluded from the system. Bacteria within the biofilm did not co-aggregate but formed discrete, species-specific clusters. Biofilms demonstrated differential tolerance to the topical antimicrobials Neosporin and HOCl, consistent with protection due to the biofilm lifestyle. The characteristics exhibited within this model match those of real-world wound biofilms, reflecting the clinical scenario and yielding a powerful in vitro tool that is versatile, inexpensive, and pivotal for understanding chronic wound infection. MDPI 2023-01-10 /pmc/articles/PMC9862141/ /pubmed/36678466 http://dx.doi.org/10.3390/pathogens12010118 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Khalid, Ammara
Cookson, Alan R.
Whitworth, David E.
Beeton, Michael L.
Robins, Lori I.
Maddocks, Sarah E.
A Synthetic Polymicrobial Community Biofilm Model Demonstrates Spatial Partitioning, Tolerance to Antimicrobial Treatment, Reduced Metabolism, and Small Colony Variants Typical of Chronic Wound Biofilms
title A Synthetic Polymicrobial Community Biofilm Model Demonstrates Spatial Partitioning, Tolerance to Antimicrobial Treatment, Reduced Metabolism, and Small Colony Variants Typical of Chronic Wound Biofilms
title_full A Synthetic Polymicrobial Community Biofilm Model Demonstrates Spatial Partitioning, Tolerance to Antimicrobial Treatment, Reduced Metabolism, and Small Colony Variants Typical of Chronic Wound Biofilms
title_fullStr A Synthetic Polymicrobial Community Biofilm Model Demonstrates Spatial Partitioning, Tolerance to Antimicrobial Treatment, Reduced Metabolism, and Small Colony Variants Typical of Chronic Wound Biofilms
title_full_unstemmed A Synthetic Polymicrobial Community Biofilm Model Demonstrates Spatial Partitioning, Tolerance to Antimicrobial Treatment, Reduced Metabolism, and Small Colony Variants Typical of Chronic Wound Biofilms
title_short A Synthetic Polymicrobial Community Biofilm Model Demonstrates Spatial Partitioning, Tolerance to Antimicrobial Treatment, Reduced Metabolism, and Small Colony Variants Typical of Chronic Wound Biofilms
title_sort synthetic polymicrobial community biofilm model demonstrates spatial partitioning, tolerance to antimicrobial treatment, reduced metabolism, and small colony variants typical of chronic wound biofilms
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9862141/
https://www.ncbi.nlm.nih.gov/pubmed/36678466
http://dx.doi.org/10.3390/pathogens12010118
work_keys_str_mv AT khalidammara asyntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT cooksonalanr asyntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT whitworthdavide asyntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT beetonmichaell asyntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT robinslorii asyntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT maddockssarahe asyntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT khalidammara syntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT cooksonalanr syntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT whitworthdavide syntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT beetonmichaell syntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT robinslorii syntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms
AT maddockssarahe syntheticpolymicrobialcommunitybiofilmmodeldemonstratesspatialpartitioningtolerancetoantimicrobialtreatmentreducedmetabolismandsmallcolonyvariantstypicalofchronicwoundbiofilms