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Adding a new dimension: Multi-level structure and organization of mixed-species Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a 4-D wound microenvironment
Biofilms in wounds typically consist of aggregates of bacteria, most often Pseudomonas aeruginosa and Staphylococcus aureus, in close association with each other and the host microenvironment. Given this, the interplay across host and microbial elements, including the biochemical and nutrient profil...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Elsevier
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9618786/ https://www.ncbi.nlm.nih.gov/pubmed/36324526 http://dx.doi.org/10.1016/j.bioflm.2022.100087 |
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author | Dhekane, Radhika Mhade, Shreeya Kaushik, Karishma S. |
author_facet | Dhekane, Radhika Mhade, Shreeya Kaushik, Karishma S. |
author_sort | Dhekane, Radhika |
collection | PubMed |
description | Biofilms in wounds typically consist of aggregates of bacteria, most often Pseudomonas aeruginosa and Staphylococcus aureus, in close association with each other and the host microenvironment. Given this, the interplay across host and microbial elements, including the biochemical and nutrient profile of the microenvironment, likely influences the structure and organization of wound biofilms. While clinical studies, in vivo and ex vivo model systems have provided insights into the distribution of P. aeruginosa and S. aureus in wounds, they are limited in their ability to provide a detailed characterization of biofilm structure and organization across the host-microbial interface. On the other hand, biomimetic in vitro systems, such as host cell surfaces and simulant media conditions, albeit reductionist, have been shown to support the co-existence of P. aeruginosa and S. aureus biofilms, with species-dependent localization patterns and interspecies interactions. Therefore, composite in vitro models that bring together key features of the wound microenvironment could provide unprecedented insights into the structure and organization of mixed-species biofilms. We have built a four-dimensional (4-D) wound microenvironment consisting of a 3-D host cell scaffold of co-cultured human epidermal keratinocytes and dermal fibroblasts, and an in vitro wound milieu (IVWM); the IVWM provides the fourth dimension that represents the biochemical and nutrient profile of the wound infection state. We leveraged this 4-D wound microenvironment, in comparison with biofilms in IVWM alone and standard laboratory media, to probe the structure of mixed-species P. aeruginosa and S. aureus biofilms across multiple levels of organization such as aggregate dimensions and biomass thickness, species co-localization and spatial organization within the biomass, overall biomass composition and interspecies interactions. In doing so, the 4-D wound microenvironment platform provides multi-level insights into the structure of mixed-species biofilms, which we incorporate into the current understanding of P. aeruginosa and S. aureus organization in the wound bed. |
format | Online Article Text |
id | pubmed-9618786 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Elsevier |
record_format | MEDLINE/PubMed |
spelling | pubmed-96187862022-11-01 Adding a new dimension: Multi-level structure and organization of mixed-species Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a 4-D wound microenvironment Dhekane, Radhika Mhade, Shreeya Kaushik, Karishma S. Biofilm Article Biofilms in wounds typically consist of aggregates of bacteria, most often Pseudomonas aeruginosa and Staphylococcus aureus, in close association with each other and the host microenvironment. Given this, the interplay across host and microbial elements, including the biochemical and nutrient profile of the microenvironment, likely influences the structure and organization of wound biofilms. While clinical studies, in vivo and ex vivo model systems have provided insights into the distribution of P. aeruginosa and S. aureus in wounds, they are limited in their ability to provide a detailed characterization of biofilm structure and organization across the host-microbial interface. On the other hand, biomimetic in vitro systems, such as host cell surfaces and simulant media conditions, albeit reductionist, have been shown to support the co-existence of P. aeruginosa and S. aureus biofilms, with species-dependent localization patterns and interspecies interactions. Therefore, composite in vitro models that bring together key features of the wound microenvironment could provide unprecedented insights into the structure and organization of mixed-species biofilms. We have built a four-dimensional (4-D) wound microenvironment consisting of a 3-D host cell scaffold of co-cultured human epidermal keratinocytes and dermal fibroblasts, and an in vitro wound milieu (IVWM); the IVWM provides the fourth dimension that represents the biochemical and nutrient profile of the wound infection state. We leveraged this 4-D wound microenvironment, in comparison with biofilms in IVWM alone and standard laboratory media, to probe the structure of mixed-species P. aeruginosa and S. aureus biofilms across multiple levels of organization such as aggregate dimensions and biomass thickness, species co-localization and spatial organization within the biomass, overall biomass composition and interspecies interactions. In doing so, the 4-D wound microenvironment platform provides multi-level insights into the structure of mixed-species biofilms, which we incorporate into the current understanding of P. aeruginosa and S. aureus organization in the wound bed. Elsevier 2022-10-20 /pmc/articles/PMC9618786/ /pubmed/36324526 http://dx.doi.org/10.1016/j.bioflm.2022.100087 Text en © 2022 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
spellingShingle | Article Dhekane, Radhika Mhade, Shreeya Kaushik, Karishma S. Adding a new dimension: Multi-level structure and organization of mixed-species Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a 4-D wound microenvironment |
title | Adding a new dimension: Multi-level structure and organization of mixed-species Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a 4-D wound microenvironment |
title_full | Adding a new dimension: Multi-level structure and organization of mixed-species Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a 4-D wound microenvironment |
title_fullStr | Adding a new dimension: Multi-level structure and organization of mixed-species Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a 4-D wound microenvironment |
title_full_unstemmed | Adding a new dimension: Multi-level structure and organization of mixed-species Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a 4-D wound microenvironment |
title_short | Adding a new dimension: Multi-level structure and organization of mixed-species Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a 4-D wound microenvironment |
title_sort | adding a new dimension: multi-level structure and organization of mixed-species pseudomonas aeruginosa and staphylococcus aureus biofilms in a 4-d wound microenvironment |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9618786/ https://www.ncbi.nlm.nih.gov/pubmed/36324526 http://dx.doi.org/10.1016/j.bioflm.2022.100087 |
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