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Salmonella Biofilm Formation on Aspergillus niger Involves Cellulose – Chitin Interactions

Salmonella cycles between host and nonhost environments, where it can become an active member of complex microbial communities. The role of fungi in the environmental adaptation of enteric pathogens remains relatively unexplored. We have discovered that S. enterica Typhimurium rapidly attaches to an...

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Autores principales: Brandl, Maria T., Carter, Michelle Q., Parker, Craig T., Chapman, Matthew R., Huynh, Steven, Zhou, Yaguang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3189214/
https://www.ncbi.nlm.nih.gov/pubmed/22003399
http://dx.doi.org/10.1371/journal.pone.0025553
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author Brandl, Maria T.
Carter, Michelle Q.
Parker, Craig T.
Chapman, Matthew R.
Huynh, Steven
Zhou, Yaguang
author_facet Brandl, Maria T.
Carter, Michelle Q.
Parker, Craig T.
Chapman, Matthew R.
Huynh, Steven
Zhou, Yaguang
author_sort Brandl, Maria T.
collection PubMed
description Salmonella cycles between host and nonhost environments, where it can become an active member of complex microbial communities. The role of fungi in the environmental adaptation of enteric pathogens remains relatively unexplored. We have discovered that S. enterica Typhimurium rapidly attaches to and forms biofilms on the hyphae of the common fungus, Aspergillus niger. Several Salmonella enterica serovars displayed a similar interaction, whereas other bacterial species were unable to bind to the fungus. Bacterial attachment to chitin, a major constituent of fungal cell walls, mirrored this specificity. Pre-incubation of S. Typhimurium with N-acetylglucosamine, the monomeric component of chitin, reduced binding to chitin beads by as much as 727-fold and inhibited attachment to A. niger hyphae considerably. A cellulose-deficient mutant of S. Typhimurium failed to attach to chitin beads and to the fungus. Complementation of this mutant with the cellulose operon restored binding to chitin beads to 79% of that of the parental strain and allowed for attachment and biofilm formation on A. niger, indicating that cellulose is involved in bacterial attachment to the fungus via the chitin component of its cell wall. In contrast to cellulose, S. Typhimurium curli fimbriae were not required for attachment and biofilm development on the hyphae but were critical for its stability. Our results suggest that cellulose–chitin interactions are required for the production of mixed Salmonella-A. niger biofilms, and support the hypothesis that encounters with chitinaceous alternate hosts may contribute to the ecological success of human pathogens.
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spelling pubmed-31892142011-10-14 Salmonella Biofilm Formation on Aspergillus niger Involves Cellulose – Chitin Interactions Brandl, Maria T. Carter, Michelle Q. Parker, Craig T. Chapman, Matthew R. Huynh, Steven Zhou, Yaguang PLoS One Research Article Salmonella cycles between host and nonhost environments, where it can become an active member of complex microbial communities. The role of fungi in the environmental adaptation of enteric pathogens remains relatively unexplored. We have discovered that S. enterica Typhimurium rapidly attaches to and forms biofilms on the hyphae of the common fungus, Aspergillus niger. Several Salmonella enterica serovars displayed a similar interaction, whereas other bacterial species were unable to bind to the fungus. Bacterial attachment to chitin, a major constituent of fungal cell walls, mirrored this specificity. Pre-incubation of S. Typhimurium with N-acetylglucosamine, the monomeric component of chitin, reduced binding to chitin beads by as much as 727-fold and inhibited attachment to A. niger hyphae considerably. A cellulose-deficient mutant of S. Typhimurium failed to attach to chitin beads and to the fungus. Complementation of this mutant with the cellulose operon restored binding to chitin beads to 79% of that of the parental strain and allowed for attachment and biofilm formation on A. niger, indicating that cellulose is involved in bacterial attachment to the fungus via the chitin component of its cell wall. In contrast to cellulose, S. Typhimurium curli fimbriae were not required for attachment and biofilm development on the hyphae but were critical for its stability. Our results suggest that cellulose–chitin interactions are required for the production of mixed Salmonella-A. niger biofilms, and support the hypothesis that encounters with chitinaceous alternate hosts may contribute to the ecological success of human pathogens. Public Library of Science 2011-10-07 /pmc/articles/PMC3189214/ /pubmed/22003399 http://dx.doi.org/10.1371/journal.pone.0025553 Text en This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
spellingShingle Research Article
Brandl, Maria T.
Carter, Michelle Q.
Parker, Craig T.
Chapman, Matthew R.
Huynh, Steven
Zhou, Yaguang
Salmonella Biofilm Formation on Aspergillus niger Involves Cellulose – Chitin Interactions
title Salmonella Biofilm Formation on Aspergillus niger Involves Cellulose – Chitin Interactions
title_full Salmonella Biofilm Formation on Aspergillus niger Involves Cellulose – Chitin Interactions
title_fullStr Salmonella Biofilm Formation on Aspergillus niger Involves Cellulose – Chitin Interactions
title_full_unstemmed Salmonella Biofilm Formation on Aspergillus niger Involves Cellulose – Chitin Interactions
title_short Salmonella Biofilm Formation on Aspergillus niger Involves Cellulose – Chitin Interactions
title_sort salmonella biofilm formation on aspergillus niger involves cellulose – chitin interactions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3189214/
https://www.ncbi.nlm.nih.gov/pubmed/22003399
http://dx.doi.org/10.1371/journal.pone.0025553
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