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Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies

Indoor surfaces are paradoxically presumed to be both colonized by pathogens, necessitating disinfection, and “microbial wastelands.” In these resource-poor, dry environments, competition and decay are thought to be important drivers of microbial community composition. However, the relative contribu...

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Autores principales: Hu, Jinglin, Shuai, Weitao, Sumner, Jack T., Moghadam, Anahid A., Hartmann, Erica M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9485146/
https://www.ncbi.nlm.nih.gov/pubmed/36123373
http://dx.doi.org/10.1038/s41522-022-00335-7
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author Hu, Jinglin
Shuai, Weitao
Sumner, Jack T.
Moghadam, Anahid A.
Hartmann, Erica M.
author_facet Hu, Jinglin
Shuai, Weitao
Sumner, Jack T.
Moghadam, Anahid A.
Hartmann, Erica M.
author_sort Hu, Jinglin
collection PubMed
description Indoor surfaces are paradoxically presumed to be both colonized by pathogens, necessitating disinfection, and “microbial wastelands.” In these resource-poor, dry environments, competition and decay are thought to be important drivers of microbial community composition. However, the relative contributions of these two processes have not been specifically evaluated. To bridge this knowledge gap, we used microcosms to evaluate whether interspecies interactions occur on surfaces. We combined transcriptomics and traditional microbiology techniques to investigate whether competition occurred between two clinically important pathogens, Acinetobacter baumannii and Klebsiella pneumoniae, and a probiotic cleaner containing a consortium of Bacillus species. Probiotic cleaning seeks to take advantage of ecological principles such as competitive exclusion, thus using benign microorganisms to inhibit viable pathogens, but there is limited evidence that competitive exclusion in fact occurs in environments of interest (i.e., indoor surfaces). Our results indicate that competition in this setting has a negligible impact on community composition but may influence the functions expressed by active organisms. Although Bacillus spp. remained viable on surfaces for an extended period of time after application, viable colony forming units (CFUs) of A. baumannii recovered following exposure to a chemical-based detergent with and without Bacillus spp. showed no statistical difference. Similarly, for K. pneumoniae, there were small statistical differences in CFUs between cleaning scenarios with or without Bacillus spp. in the chemical-based detergent. The transcriptome of A. baumannii with and without Bacillus spp. exposure shared a high degree of similarity in overall gene expression, but the transcriptome of K. pneumoniae differed in overall gene expression, including reduced response in genes related to antimicrobial resistance. Together, these results highlight the need to fully understand the underlying biological and ecological mechanisms for community assembly and function on indoor surfaces, as well as having practical implications for cleaning and disinfection strategies for infection prevention.
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spelling pubmed-94851462022-09-21 Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies Hu, Jinglin Shuai, Weitao Sumner, Jack T. Moghadam, Anahid A. Hartmann, Erica M. NPJ Biofilms Microbiomes Article Indoor surfaces are paradoxically presumed to be both colonized by pathogens, necessitating disinfection, and “microbial wastelands.” In these resource-poor, dry environments, competition and decay are thought to be important drivers of microbial community composition. However, the relative contributions of these two processes have not been specifically evaluated. To bridge this knowledge gap, we used microcosms to evaluate whether interspecies interactions occur on surfaces. We combined transcriptomics and traditional microbiology techniques to investigate whether competition occurred between two clinically important pathogens, Acinetobacter baumannii and Klebsiella pneumoniae, and a probiotic cleaner containing a consortium of Bacillus species. Probiotic cleaning seeks to take advantage of ecological principles such as competitive exclusion, thus using benign microorganisms to inhibit viable pathogens, but there is limited evidence that competitive exclusion in fact occurs in environments of interest (i.e., indoor surfaces). Our results indicate that competition in this setting has a negligible impact on community composition but may influence the functions expressed by active organisms. Although Bacillus spp. remained viable on surfaces for an extended period of time after application, viable colony forming units (CFUs) of A. baumannii recovered following exposure to a chemical-based detergent with and without Bacillus spp. showed no statistical difference. Similarly, for K. pneumoniae, there were small statistical differences in CFUs between cleaning scenarios with or without Bacillus spp. in the chemical-based detergent. The transcriptome of A. baumannii with and without Bacillus spp. exposure shared a high degree of similarity in overall gene expression, but the transcriptome of K. pneumoniae differed in overall gene expression, including reduced response in genes related to antimicrobial resistance. Together, these results highlight the need to fully understand the underlying biological and ecological mechanisms for community assembly and function on indoor surfaces, as well as having practical implications for cleaning and disinfection strategies for infection prevention. Nature Publishing Group UK 2022-09-19 /pmc/articles/PMC9485146/ /pubmed/36123373 http://dx.doi.org/10.1038/s41522-022-00335-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hu, Jinglin
Shuai, Weitao
Sumner, Jack T.
Moghadam, Anahid A.
Hartmann, Erica M.
Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies
title Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies
title_full Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies
title_fullStr Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies
title_full_unstemmed Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies
title_short Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies
title_sort clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9485146/
https://www.ncbi.nlm.nih.gov/pubmed/36123373
http://dx.doi.org/10.1038/s41522-022-00335-7
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