Development and application of a polymicrobial, in vitro, wound biofilm model

Woods, Janet; Boegli, Laura; Kirker, Kelly R.; Agostinho, Alessandra Marçal; Durch, Amanda M.; Pulcini, Elinor deLancey; Stewart, Philip S.; James, Garth A.

doi:10.1111/j.1365-2672.2012.05264.x

Cited by 62 publications

(58 citation statements)

References 35 publications

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“…Due to the varying oxygen content found in chronic wounds, an in vitro wound model using a drip flow reactor and 5% bovine serum was used to investigate the role of strict anaerobes in wound-like environments [59]. Common wound pathogens P. aeruginosa and methicillin-resistant S. aureus and the obligate anaerobe Clostridium perfringens, were used to establish a unique anaerobic environment that allowed for the growth of C. perfringens under otherwise prohibitory conditions.…”

Section: Notable Polymicrobial Studies In Dynamic Systemsmentioning

confidence: 99%

“…This experimental setup simulated the temperature, pH, flow and anaerobic conditions of the oral cavity and included a tooth surface (hydroxyapatite) for attachment. The investigators used this model to investigate interactions between primary, intermediate and late colonizers during the progression of oral infections.Due to the varying oxygen content found in chronic wounds, an in vitro wound model using a drip flow reactor and 5% bovine serum was used to investigate the role of strict anaerobes in wound-like environments [59]. Common wound pathogens P. aeruginosa and methicillin-resistant S. aureus and the obligate anaerobe Clostridium perfringens, were used to establish a unique anaerobic environment that allowed for the growth of C. perfringens under otherwise prohibitory conditions.…”

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confidence: 99%

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Biofilm Models of Polymicrobial Infection

2015

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Interactions between microbes are complex and play an important role in the pathogenesis of infections. These interactions can range from fierce competition for nutrients and niches to highly evolved cooperative mechanisms between different species that support their mutual growth. An increasing appreciation for these interactions, and desire to uncover the mechanisms that govern them, has resulted in a shift from monomicrobial to polymicrobial biofilm studies in different disease models. Here we provide an overview of biofilm models used to study select polymicrobial infections and highlight the impact that the interactions between microbes within these biofilms have on disease progression. Notable recent advances in the development of polymicrobial biofilm-associated infection models and challenges facing the study of polymicrobial biofilms are addressed. Polymicrobial interactions in biofilmsOver the past 2 decades there has been a revolutionary paradigm shift in the field of microbiology with the appreciation that bacteria present in most biological systems exist in biofilms, rather than in a free-living state. This understanding has dramatically changed the way we study bacteria in the laboratory and resulted in the development of many new experimental systems that replicate biofilm environments [1][2][3][4][5]. Studies utilizing these systems have demonstrated time and time again that bacteria behave very differently when in a biofilm than during planktonic growth. In many ways, we now have to relearn everything we thought we knew about bacterial behavior through the view of the biofilm lens.Similarly, the recent explosion of metagenomic studies has significantly increased our appreciation of the complexity of the microbial populations present in biofilms [6,7]. This is also true for infections, most of which are thought to be biofilm related and inherently polymicrobial, including various species of bacteria, fungi and viruses [8]. It is thought that microbes act in concert to establish biofilms, which in turn can increase tolerance to antimicrobials, exacerbate of the host's immune response and increase persistence at the infection site [7,[9][10][11].Genetic diversity of microbes within biofilm communities is thought to increase the fitness of the residing community, making them more equipped to survive environmental stresses. In large part, this is due to an expanded gene pool, which can be more easily shared within the confines of a biofilm community [12]. Community composition and interactions within the community can have huge influences on bacterial behavior. Thus, just as the behavior of planktonic versus biofilm-associated bacteria is dramatically different, so is that of bacteria in single species versus multispecies systems.Interactions between microbes are complex and highly dependent on context. They can range from fierce competition for nutrients and niches, manifested by antagonistic behavior, to highly evolved cooperative mechanisms between different species that support their mutual grow...

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Section: Notable Polymicrobial Studies In Dynamic Systemsmentioning

confidence: 99%

mentioning

confidence: 99%

Biofilm Models of Polymicrobial Infection

2015

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“…The presence of spatial heterogeneity within biofilms plays an essential role in the evolution and function of microbial species [2,[6][7][8][9] and has profound effects on biofilm formation and development [5,[10][11][12]. Concentration gradients in key nutrients due to limited diffusion can establish metabolic niches within the biofilm which produce spatial variations in biomass density [13] and partitioning of species [14]. With their inherent chemical gradients, biofilms can provide niches for both fast and slow growing organisms, a design feature thought to be critical to the stability of naturally occurring systems.…”

Section: Introductionmentioning

confidence: 99%

Byproduct Cross Feeding and Community Stability in an In Silico Biofilm Model of the Gut Microbiome

Henson

Phalak

2017

Processes

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Abstract:The gut microbiome is a highly complex microbial community that strongly impacts human health and disease. The two dominant phyla in healthy humans are Bacteroidetes and Firmicutes, with minor phyla such as Proteobacteria having elevated abundances in various disease states. While the gut microbiome has been widely studied, relatively little is known about the role of interspecies interactions in promoting microbiome stability and function. We developed a biofilm metabolic model of a very simple gut microbiome community consisting of a representative bacteroidete (Bacteroides thetaiotaomicron), firmicute (Faecalibacterium prausnitzii) and proteobacterium (Escherichia coli) to investigate the putative role of metabolic byproduct cross feeding between species on community stability, robustness and flexibility. The model predicted coexistence of the three species only if four essential cross-feeding relationships were present. We found that cross feeding allowed coexistence to be robustly maintained for large variations in biofilm thickness and nutrient levels. However, the model predicted that community composition and short chain fatty acid levels could be strongly affected only over small ranges of byproduct uptake rates, indicating a possible lack of flexibility in our cross-feeding mechanism. Our model predictions provide new insights into the impact of byproduct cross feeding and yield experimentally testable hypotheses about gut microbiome community stability.

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“…Biofilm consortia have been engineered for wastewater treatment and bioremediation of contaminated soils, bioelectrochemical systems that convert chemical energy into electrical energy and/or the production of commodity and specialty chemicals . Numerous experimental studies have demonstrated the potential of the engineered biofilm consortia concept . Biofilm consortia offer many possible advantages for bioprocess applications, including the ability to achieve high cell densities (200–300 gDW L −1 ), which can lead to high volumetric productivities in relatively small bioreactors, no requirement for energy intensive agitation or aeration processes, efficient recovery of biomass and biomass‐associated products, and high tolerance to culturing stresses and inhibitors .…”

Section: Introductionmentioning

confidence: 99%

In Silico Metabolic Design of Two‐Strain Biofilm Systems Predicts Enhanced Biomass Production and Biochemical Synthesis

Patel

Carlson

Henson

2019

Biotechnology Journal

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Engineered biofilm consortia have the potential to solve important biotechnological problems that have proved difficult for monoculture biofilms and planktonic consortia, such as conversion of lignocellulosic material to useful biochemicals. While considerable experimental progress has been reported for engineering and characterizing biofilm consortia, the field still lacks in silico tools for simulation, design, and optimization of stable, robust, and productive designed consortia. We developed biofilm consortia metabolic models for two coculture systems centered around the ecological design motif of a primary cell type that utilizes a supplied electron donor and secretes acetate as a byproduct and a secondary cell type that consumes the acetate, relieving byproduct inhibition on the primary cell type and enhancing overall system biomass. The models presented in this paper predict that distinct metabolic niches for the two cell types could be established by supplying electron donors and acceptors at opposite ends of the biofilm and that acetate consumption by the secondary cell type could increase total biomass accumulation and the synthesis of valuable biochemicals, such as isobutanol, by the primary cell type. System tunability is enhanced when each cell type is supplied with a unique terminal electron acceptor at opposite ends of the biofilm rather than competing for a common electron acceptor. Our model provides good qualitative agreement with data for a synthetic Escherichia coli coculture system, suggesting that the proposed design rules may have wide applicability to engineered biofilm consortia.

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Development and application of a polymicrobial, in vitro, wound biofilm model

Cited by 62 publications

References 35 publications

Biofilm Models of Polymicrobial Infection

Biofilm Models of Polymicrobial Infection

Byproduct Cross Feeding and Community Stability in an In Silico Biofilm Model of the Gut Microbiome

In Silico Metabolic Design of Two‐Strain Biofilm Systems Predicts Enhanced Biomass Production and Biochemical Synthesis

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