Mathematical Description of Microbial Biofilms

Klapper, Isaac; Dockery, Jack D.

doi:10.1137/080739720

Cited by 172 publications

(138 citation statements)

References 254 publications

(324 reference statements)

Supporting

Mentioning

135

Contrasting

Unclassified

Order By: Relevance

“…6,8,[35][36][37][38][39][40][41][42][43]. We use the Pirt model, which interprets the linear relationship between population metabolism and growth rate as a metabolic partitioning between growth and maintenance (44) and is consistent with the physiology of a broad range of bacterial and eukaryotic species (see, e.g., refs.…”

Section: Modeling Biofilm Metabolism and Oxygen Dynamicsmentioning

confidence: 99%

Morphological optimization for access to dual oxidants in biofilms

Kempes

Okegbe

Mears-Clarke

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

A major theme driving research in biology is the relationship between form and function. In particular, a longstanding goal has been to understand how the evolution of multicellularity conferred fitness advantages. Here we show that biofilms of the bacterium Pseudomonas aeruginosa produce structures that maximize cellular reproduction. Specifically, we develop a mathematical model of resource availability and metabolic response within colony features. This analysis accurately predicts the measured distribution of two types of electron acceptors: oxygen, which is available from the atmosphere, and phenazines, redox-active antibiotics produced by the bacterium. Using this model, we demonstrate that the geometry of colony structures is optimal with respect to growth efficiency. Because our model is based on resource dynamics, we also can anticipate shifts in feature geometry based on changes to the availability of electron acceptors, including variations in the external availability of oxygen and genetic manipulation that renders the cells incapable of phenazine production.A desire to understand the relationship between form and function motivates many lines of inquiry in biology, including the study of multicellular morphologies and the evolution of these features. Cells grow and survive in populations in many types of natural systems. These multicellular populations include bacterial biofilms, such as Pseudomonas aeruginosa microcolonies in the lungs of cystic fibrosis patients (1) and cyanobacterial colonies and mats in marshes, lakes, and oceans (2, 3), and complex eukaryotic macroorganisms, such as plants and animals. In many of these contexts, enhanced survival arises from advantages associated with multicellularity at multiple scales. Recent work demonstrated that simple cooperation within aqueous microbial biofilms allows groups of genetically similar cells to form tall mushroom-like structures that reach beyond local depletion zones into areas of fresh resources (4-12). Other work has shown that basic colonial growth (e.g., that of budding yeast) and the evolution of complex multicellular life are accompanied by enhanced growth efficiency and several energetic advantages (13-15).The specific organization of and relationship between cells living within a population are important characteristics that determine whether organisms benefit from the multicellular lifestyle. For example, in mammals the metabolic rate of individual cells is regulated by the size of the whole organism, an effect that confers greater efficiency (15). Cells have dramatically elevated metabolic rates when living as individuals in culture compared with when they survive and grow as members of a multicellular organism (15). This regulation is considered a natural consequence of resource supply within hierarchical vascular networks (15-17) and highlights the importance of morphology and structure in dictating cellular physiology for multicellular systems. Variations in gross morphology also may provide information about how different spec...

show abstract

Section: Modeling Biofilm Metabolism and Oxygen Dynamicsmentioning

confidence: 99%

Morphological optimization for access to dual oxidants in biofilms

Kempes

Okegbe

Mears-Clarke

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…Thus far, these studies have predominantly focused on selective pressures acting at the level of the individual cell. However, many species live in dense, surfaceassociated communities known as biofilms, which are fundamental to the biology of microbes and how they affect us-playing major roles in the human microbiome, chronic diseases, antibiotic resistance, biofouling, and waste-water treatment (13)(14)(15)(16)(17). As a result, there has been an intensive effort in recent years to understand how the biofilm mode of growth affects microbes and their evolution (18,19), but we know very little of the importance of cell shape for biofilm biology.…”

mentioning

confidence: 99%

Cell morphology drives spatial patterning in microbial communities

Smith

Davit

Osborne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

156

138

View full text Add to dashboard Cite

The clearest phenotypic characteristic of microbial cells is their shape, but we do not understand how cell shape affects the dense communities, known as biofilms, where many microbes live. Here, we use individual-based modeling to systematically vary cell shape and study its impact in simulated communities. We compete cells with different cell morphologies under a range of conditions and ask how shape affects the patterning and evolutionary fitness of cells within a community. Our models predict that cell shape will strongly influence the fate of a cell lineage: we describe a mechanism through which coccal (round) cells rise to the upper surface of a community, leading to a strong spatial structuring that can be critical for fitness. We test our predictions experimentally using strains of Escherichia coli that grow at a similar rate but differ in cell shape due to single amino acid changes in the actin homolog MreB. As predicted by our model, cell types strongly sort by shape, with round cells at the top of the colony and rod cells dominating the basal surface and edges. Our work suggests that cell morphology has a strong impact within microbial communities and may offer new ways to engineer the structure of synthetic communities.biofilms | cell morphology | biophysics | self-organization | synthetic biology S ingle-celled microorganisms such as bacteria display significant morphological diversity, ranging from the simple to the complex and exotic (1-3). Phylogenetic studies indicate that particular morphologies have evolved independently multiple times, suggesting that the myriad shapes of modern bacteria may be adaptations to particular environments (4-6). Microbes can also actively change their morphology in response to environmental stimuli, such as changes to nutrient levels or predation (7,8). However, understanding when and why particular cell shapes offer a competitive edge remains an unresolved question in microbiology.Previous studies have characterized selective pressures favoring particular shapes (7, 9-11): for example, highly viscous environments may select for the helical cell morphologies observed in spirochete bacteria (12). Thus far, these studies have predominantly focused on selective pressures acting at the level of the individual cell. However, many species live in dense, surfaceassociated communities known as biofilms, which are fundamental to the biology of microbes and how they affect us-playing major roles in the human microbiome, chronic diseases, antibiotic resistance, biofouling, and waste-water treatment (13-17). As a result, there has been an intensive effort in recent years to understand how the biofilm mode of growth affects microbes and their evolution (18, 19), but we know very little of the importance of cell shape for biofilm biology.In biofilms, microbial cells are often in close physical contact, making mechanical interactions between neighboring cells particularly significant. Recent studies have suggested that rodshaped cells can drive collective behaviors in microbial g...

show abstract

“…In time, models have increased in dimension (2D and 3D) and have made use of individual-based modeling (IBM) [37,38] to more concisely describe the heterogeneous behavior commonly observed within a biofilm [35,39]. Although growth remains the primary focus of many biofilm models, other factors such as quorum sensing [35,40] and biofilm mechanics [35,41] have also been represented. To elucidate the features of a microbial biofilm model, the 3D simulation of a biofilm on porous media [42][43][44] or in unsaturated soil [45] has been considered.…”

Section: Spatial Modelsmentioning

confidence: 99%

“…These types of models were initially one-dimensional and incorporated reaction-diffusion equations for nutrients and other cell-produced compounds [35,36]. In time, models have increased in dimension (2D and 3D) and have made use of individual-based modeling (IBM) [37,38] to more concisely describe the heterogeneous behavior commonly observed within a biofilm [35,39]. Although growth remains the primary focus of many biofilm models, other factors such as quorum sensing [35,40] and biofilm mechanics [35,41] have also been represented.…”

Section: Spatial Modelsmentioning

confidence: 99%

See 1 more Smart Citation

Modeling Microbial Communities: A Call for Collaboration between Experimentalists and Theorists

2017

View full text Add to dashboard Cite

With our growing understanding of the impact of microbial communities, understanding how such communities function has become a priority. The influence of microbial communities is widespread. Human-associated microbiota impacts health, environmental microbes determine ecosystem sustainability, and microbe-driven industrial processes are expanding. This broad range of applications has led to a wide range of approaches to analyze and describe microbial communities. In particular, theoretical work based on mathematical modeling has been a steady source of inspiration for explaining and predicting microbial community processes. Here, we survey some of the modeling approaches used in different contexts. We promote classifying different approaches using a unified platform, and encourage cataloging the findings in a database. We believe that the synergy emerging from a coherent collection facilitates a better understanding of important processes that determine microbial community functions. We emphasize the importance of close collaboration between theoreticians and experimentalists in formulating, classifying, and improving models of microbial communities.

show abstract

Mathematical Description of Microbial Biofilms

Abstract: We describe microbial communities denoted biofilms and efforts to model some of their important aspects, including quorum sensing, growth, mechanics, and antimicrobial tolerance mechanisms.

Cited by 172 publications

References 254 publications

Morphological optimization for access to dual oxidants in biofilms

Morphological optimization for access to dual oxidants in biofilms

Cell morphology drives spatial patterning in microbial communities

Modeling Microbial Communities: A Call for Collaboration between Experimentalists and Theorists

Contact Info

Product

Resources

About