Continuous versus Arrested Spreading of Biofilms at Solid-Gas Interfaces: The Role of Surface Forces

Trinschek, Sarah; John, Karin; Lecuyer, Sigolène; Thiele, Uwe

doi:10.1103/physrevlett.119.078003

Cited by 34 publications

(48 citation statements)

References 40 publications

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“…Recent theoretical approaches have considered specific physical factors such as the wettability of the biofilm (Trinschek et al, 2016; Trinschek et al, 2017), osmotic pressure in the EPS matrix (Winstanley et al, 2011; Seminara et al, 2012), or Marangoni stresses associated with the swarm fluid (Fauvart et al, 2012), as reviewed by Allen and Waclaw (2019). However, a description that captures the experimental observations described in Figure 1 remains lacking.…”

Section: Theoretical Frameworkmentioning

confidence: 99%

A multiphase theory for spreading microbial swarms and films

Srinivasan

Kaplan

Mahadevan

2019

eLife

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Bacterial swarming and biofilm formation are collective multicellular phenomena through which diverse microbial species colonize and spread over water-permeable tissue. During both modes of surface translocation, fluid uptake and transport play a key role in shaping the overall morphology and spreading dynamics. Here we develop a generalized two-phase thin-film model that couples bacterial growth, extracellular matrix swelling, fluid flow, and nutrient transport to describe the expansion of both highly motile bacterial swarms, and sessile bacterial biofilms. We show that swarm expansion corresponds to steady-state solutions in a nutrient-rich, capillarity dominated regime. In contrast, biofilm colony growth is described by transient solutions associated with a nutrient-limited, extracellular polymer stress driven limit. We apply our unified framework to explain a range of recent experimental observations of steady and unsteady expansion of microbial swarms and biofilms. Our results demonstrate how the physics of flow and transport in slender geometries serve to constrain biological organization in microbial communities.

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Section: Theoretical Frameworkmentioning

confidence: 99%

A multiphase theory for spreading microbial swarms and films

Srinivasan

Kaplan

Mahadevan

2019

eLife

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“…In both natural and experimental settings, organisms contribute to the reconstruction of the interspecies niche (Miner, Sultan, Morgan, Padilla, & Relyea, ; Ryan, Powers, & Watson, ). For instance, bacterial extracellular matrix secretion is altered by the medium mechanical properties, which in turn are altered by the extracellular matrix secretion (Be'er et al, ; Fauvart et al, ; Rivera‐Yoshida et al, ; Trinschek, John, Lecuyer, & Thiele, ). Thus, dynamics associated with natural and experimental settings cannot be fully compared as they follow their own evolutionary tempos and paths.…”

Section: Laboratory Settings Versus Natural Environmentsmentioning

confidence: 99%

Laboratory biases hinder Eco‐Evo‐Devo integration: Hints from the microbial world

et al. 2019

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How specific environmental contexts contribute to the robustness and variation of developmental trajectories and evolutionary transitions is a central point in Ecological Evolutionary Developmental Biology (“Eco‐Evo‐Devo”). However, the articulation of ecological, evolutionary and developmental processes into integrative frameworks has been elusive, partly because standard experimental designs neglect or oversimplify ecologically meaningful contexts. Microbial models are useful to expose and discuss two possible sources of bias associated with conventional gene‐centered experimental designs: the use of laboratory strains and standard laboratory environmental conditions. We illustrate our point by showing how contrasting developmental phenotypes in Myxococcus xanthus depend on the joint variation of temperature and substrate stiffness. Microorganismal development can provide key information for better understanding the role of environmental conditions in the evolution of developmental variation, and to overcome some of the limitations associated with current experimental approaches.

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“…Under some conditions, the extracellular matrix holds cells together tightly and promotes either vertical buckling (18) or out-of-plane growth (19) that manifests as colony wrinkling. The formation of some B. subtilis biofilm wrinkles has been associated with mechanical stresses (20) resulting from mechanical forces directed at sites of cell death (21) or as a result of self-produced chemical gradients (22). The primary structural components of B. subtilis extracellular matrix are an exopolysaccharide (EPS, encoded by the operon epsA-O), the protein TasA, which assembles into fibers attached to the cell wall and provides structural integrity to the biofilm (23,24), and the protein BslA, which provides a hydrophobic coat to the surface of the biofilm (25).…”

mentioning

confidence: 99%

A Dual-Species Biofilm with Emergent Mechanical and Protective Properties

et al. 2019

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Many microbes coexist within biofilms, or multispecies communities of cells encased in an extracellular matrix. However, little is known about the microbemicrobe interactions relevant for creating these structures. In this study, we explored a striking dual-species biofilm between Bacillus subtilis and Pantoea agglomerans that exhibited characteristics that were not predictable from previous work examining monoculture biofilms. Coculture wrinkle formation required a P. agglomerans exopolysaccharide as well as the B. subtilis amyloid-like protein TasA. Unexpectedly, other B. subtilis matrix components essential for monoculture biofilm formation were not necessary for coculture wrinkling (e.g., the exopolysaccharide EPS, the hydrophobin BslA, and cell chaining). In addition, B. subtilis cell chaining prevented coculture wrinkling, even though chaining was previously associated with more robust monoculture biofilms. We also observed that increasing the relative proportion of P. agglomerans (which forms completely featureless monoculture colonies) increased coculture wrinkling. Using microscopy and rheology, we observed that these two bacteria assemble into an organized layered structure that reflects the physical properties of both monocultures. This partitioning into distinct regions negatively affected the survival of P. agglomerans while also serving as a protective mechanism in the presence of antibiotic stress. Taken together, these data indicate that studying cocultures is a productive avenue to identify novel mechanisms that drive the formation of structured microbial communities. IMPORTANCE In the environment, many microbes form biofilms. However, the interspecies interactions underlying bacterial coexistence within these biofilms remain understudied. Here, we mimic environmentally relevant biofilms by studying a dualspecies biofilm formed between Bacillus subtilis and Pantoea agglomerans and subjecting the coculture to chemical and physical stressors that it may experience in the natural world. We determined that both bacteria contribute structural elements to the coculture, which is reflected in its overall viscoelastic behavior. Existence within the coculture can be either beneficial or detrimental depending on the context. Many of the features and determinants of the coculture biofilm appear distinct from those identified in monoculture biofilm studies, highlighting the importance of characterizing multispecies consortia to understand naturally occurring bacterial interactions.

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Continuous versus Arrested Spreading of Biofilms at Solid-Gas Interfaces: The Role of Surface Forces

Cited by 34 publications

References 40 publications

A multiphase theory for spreading microbial swarms and films

A multiphase theory for spreading microbial swarms and films

Laboratory biases hinder Eco‐Evo‐Devo integration: Hints from the microbial world

A Dual-Species Biofilm with Emergent Mechanical and Protective Properties

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