The role of surface adhesion on the macroscopic wrinkling of biofilms
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Evaluation Summary:
The wrinkling of growing biofilms is considered in this paper experimentally in a clever set of experiments in a microfluidic setup that reveals aspects of the onset of the wrinkling instability and the formation of hollow channels within which bacteria move. Variations in the adhesive properties of the underlying surface are shown to affect the instability. While the results will surely be of interest to researchers in a range of areas, the connection with theoretical results needs further development.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
Biofilms, bacterial communities of cells encased by a self-produced matrix, exhibit a variety of three-dimensional structures. Specifically, channel networks formed within the bulk of the biofilm have been identified to play an important role in the colonies' viability by promoting the transport of nutrients and chemicals. Here, we study channel formation and focus on the role of the adhesion of the biofilm matrix to the substrate in Pseudomonas aeruginosa biofilms grown under constant flow in microfluidic channels. We perform phase contrast and confocal laser scanning microscopy to examine the development of the biofilm structure as a function of the substrates' surface energy. The formation of the wrinkles and folds is triggered by a mechanical buckling instability, controlled by biofilm growth rate and the film’s adhesion to the substrate. The three-dimensional folding gives rise to hollow channels that rapidly increase the effective volume occupied by the biofilm and facilitate bacterial movement inside them. The experiments and analysis on mechanical instabilities for the relevant case of a bacterial biofilm grown during flow enable us to predict and control the biofilm morphology.
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Evaluation Summary:
The wrinkling of growing biofilms is considered in this paper experimentally in a clever set of experiments in a microfluidic setup that reveals aspects of the onset of the wrinkling instability and the formation of hollow channels within which bacteria move. Variations in the adhesive properties of the underlying surface are shown to affect the instability. While the results will surely be of interest to researchers in a range of areas, the connection with theoretical results needs further development.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
In this work the authors study biofilm growth and wrinkling in a controlled microfluidic setup. They argue that previous work involving such growth on agar substrates are complicated by the nature of transport within the agar and that the present arrangement simplifies the approach. Growth-induced wrinkling is a commonly observed phenomenon, and it stands to reason that the biofilm problem may be amenable to the kinds of theoretical approaches already developed.
Using confocal imaging to study the folding and wrinkling of confined, growing biofilms, the authors find a number of very interesting results, including insights into the role of compressive forces and of adhesion with the substrate in the instability. Their imaging also reveals the generation of fluid-filled channels within the biofilm complex that …
Reviewer #1 (Public Review):
In this work the authors study biofilm growth and wrinkling in a controlled microfluidic setup. They argue that previous work involving such growth on agar substrates are complicated by the nature of transport within the agar and that the present arrangement simplifies the approach. Growth-induced wrinkling is a commonly observed phenomenon, and it stands to reason that the biofilm problem may be amenable to the kinds of theoretical approaches already developed.
Using confocal imaging to study the folding and wrinkling of confined, growing biofilms, the authors find a number of very interesting results, including insights into the role of compressive forces and of adhesion with the substrate in the instability. Their imaging also reveals the generation of fluid-filled channels within the biofilm complex that contain motile bacteria.
Existing theory from many years ago on growth-induced buckling and delamination (from the metallurgical literature) is used to rationalize the experimental observations, particularly with regard to the role of adhesion.
Overall this work provides an impressive array of results that provide real insight into the basic problem of biofilm wrinkling. Yet, a quantitative connection between the experimental observations and theories of wrinkling is absent. Although there is a discussion of the prior theory, it is not presented in a manner that significantly enhances the discussion, as there are parameters undefined/unexplained (toughness, for example) and no attempt is made to connect the observed wavelength with that arising from theory.
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Reviewer #2 (Public Review):
In this paper, the authors study the buckling instability and wrinkling of a Pseudomonas aeruginosa biofilm growing on a PDMS substrate inside a rectangular microfluidic channel in the presence of fluid flow. Overall, this paper addresses a topic of growing interest - the mechanical aspects of biofilm growth - and some of its results are clearly novel, namely: (i) the control of biofilm wrinkling and the subsequent formation of a network of channels by means of the flow of nutrients and the substrate surface properties, (ii) disentangling the main driving mechanisms for wrinkling and their interplay, and (iii) the presence of swimming bacteria inside channels formed within wrinkles, whose swimming speed remains unaffected by the external flow outside the biofilm. Nonetheless, the paper contains a few …
Reviewer #2 (Public Review):
In this paper, the authors study the buckling instability and wrinkling of a Pseudomonas aeruginosa biofilm growing on a PDMS substrate inside a rectangular microfluidic channel in the presence of fluid flow. Overall, this paper addresses a topic of growing interest - the mechanical aspects of biofilm growth - and some of its results are clearly novel, namely: (i) the control of biofilm wrinkling and the subsequent formation of a network of channels by means of the flow of nutrients and the substrate surface properties, (ii) disentangling the main driving mechanisms for wrinkling and their interplay, and (iii) the presence of swimming bacteria inside channels formed within wrinkles, whose swimming speed remains unaffected by the external flow outside the biofilm. Nonetheless, the paper contains a few shortcomings, in particular regarding the underdeveloped connection to theory and a lack of detail regarding quantitative measurements, that need to be addressed.
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