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Self-Adaptation of Pseudomonas fluorescens Biofilms to Hydrodynamic Stress

In some conditions, bacteria self-organize into biofilms, supracellular structures made of a self-produced embedding matrix, mainly composed of polysaccharides, DNA, proteins, and lipids. It is known that bacteria change their colony/matrix ratio in the presence of external stimuli such as hydrodyna...

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Autores principales: Jara, Josué, Alarcón, Francisco, Monnappa, Ajay K., Santos, José Ignacio, Bianco, Valentino, Nie, Pin, Ciamarra, Massimo Pica, Canales, Ángeles, Dinis, Luis, López-Montero, Iván, Valeriani, Chantal, Orgaz, Belén
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7835673/
https://www.ncbi.nlm.nih.gov/pubmed/33510716
http://dx.doi.org/10.3389/fmicb.2020.588884
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author Jara, Josué
Alarcón, Francisco
Monnappa, Ajay K.
Santos, José Ignacio
Bianco, Valentino
Nie, Pin
Ciamarra, Massimo Pica
Canales, Ángeles
Dinis, Luis
López-Montero, Iván
Valeriani, Chantal
Orgaz, Belén
author_facet Jara, Josué
Alarcón, Francisco
Monnappa, Ajay K.
Santos, José Ignacio
Bianco, Valentino
Nie, Pin
Ciamarra, Massimo Pica
Canales, Ángeles
Dinis, Luis
López-Montero, Iván
Valeriani, Chantal
Orgaz, Belén
author_sort Jara, Josué
collection PubMed
description In some conditions, bacteria self-organize into biofilms, supracellular structures made of a self-produced embedding matrix, mainly composed of polysaccharides, DNA, proteins, and lipids. It is known that bacteria change their colony/matrix ratio in the presence of external stimuli such as hydrodynamic stress. However, little is still known about the molecular mechanisms driving this self-adaptation. In this work, we monitor structural features of Pseudomonas fluorescens biofilms grown with and without hydrodynamic stress. Our measurements show that the hydrodynamic stress concomitantly increases the cell density population and the matrix production. At short growth timescales, the matrix mediates a weak cell-cell attractive interaction due to the depletion forces originated by the polymer constituents. Using a population dynamics model, we conclude that hydrodynamic stress causes a faster diffusion of nutrients and a higher incorporation of planktonic bacteria to the already formed microcolonies. This results in the formation of more mechanically stable biofilms due to an increase of the number of crosslinks, as shown by computer simulations. The mechanical stability also relies on a change in the chemical compositions of the matrix, which becomes enriched in carbohydrates, known to display adhering properties. Overall, we demonstrate that bacteria are capable of self-adapting to hostile hydrodynamic stress by tailoring the biofilm chemical composition, thus affecting both the mesoscale structure of the matrix and its viscoelastic properties that ultimately regulate the bacteria-polymer interactions.
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spelling pubmed-78356732021-01-27 Self-Adaptation of Pseudomonas fluorescens Biofilms to Hydrodynamic Stress Jara, Josué Alarcón, Francisco Monnappa, Ajay K. Santos, José Ignacio Bianco, Valentino Nie, Pin Ciamarra, Massimo Pica Canales, Ángeles Dinis, Luis López-Montero, Iván Valeriani, Chantal Orgaz, Belén Front Microbiol Microbiology In some conditions, bacteria self-organize into biofilms, supracellular structures made of a self-produced embedding matrix, mainly composed of polysaccharides, DNA, proteins, and lipids. It is known that bacteria change their colony/matrix ratio in the presence of external stimuli such as hydrodynamic stress. However, little is still known about the molecular mechanisms driving this self-adaptation. In this work, we monitor structural features of Pseudomonas fluorescens biofilms grown with and without hydrodynamic stress. Our measurements show that the hydrodynamic stress concomitantly increases the cell density population and the matrix production. At short growth timescales, the matrix mediates a weak cell-cell attractive interaction due to the depletion forces originated by the polymer constituents. Using a population dynamics model, we conclude that hydrodynamic stress causes a faster diffusion of nutrients and a higher incorporation of planktonic bacteria to the already formed microcolonies. This results in the formation of more mechanically stable biofilms due to an increase of the number of crosslinks, as shown by computer simulations. The mechanical stability also relies on a change in the chemical compositions of the matrix, which becomes enriched in carbohydrates, known to display adhering properties. Overall, we demonstrate that bacteria are capable of self-adapting to hostile hydrodynamic stress by tailoring the biofilm chemical composition, thus affecting both the mesoscale structure of the matrix and its viscoelastic properties that ultimately regulate the bacteria-polymer interactions. Frontiers Media S.A. 2021-01-12 /pmc/articles/PMC7835673/ /pubmed/33510716 http://dx.doi.org/10.3389/fmicb.2020.588884 Text en Copyright © 2021 Jara, Alarcón, Monnappa, Santos, Bianco, Nie, Ciamarra, Canales, Dinis, López-Montero, Valeriani and Orgaz. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Jara, Josué
Alarcón, Francisco
Monnappa, Ajay K.
Santos, José Ignacio
Bianco, Valentino
Nie, Pin
Ciamarra, Massimo Pica
Canales, Ángeles
Dinis, Luis
López-Montero, Iván
Valeriani, Chantal
Orgaz, Belén
Self-Adaptation of Pseudomonas fluorescens Biofilms to Hydrodynamic Stress
title Self-Adaptation of Pseudomonas fluorescens Biofilms to Hydrodynamic Stress
title_full Self-Adaptation of Pseudomonas fluorescens Biofilms to Hydrodynamic Stress
title_fullStr Self-Adaptation of Pseudomonas fluorescens Biofilms to Hydrodynamic Stress
title_full_unstemmed Self-Adaptation of Pseudomonas fluorescens Biofilms to Hydrodynamic Stress
title_short Self-Adaptation of Pseudomonas fluorescens Biofilms to Hydrodynamic Stress
title_sort self-adaptation of pseudomonas fluorescens biofilms to hydrodynamic stress
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7835673/
https://www.ncbi.nlm.nih.gov/pubmed/33510716
http://dx.doi.org/10.3389/fmicb.2020.588884
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