Accumulation of dead cells from contact killing facilitates coexistence in bacterial biofilms.
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ABSTRACT:
SUBMITTER: Steinbach G
PROVIDER: S-EPMC7811593 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Multistrain microbial communities often exhibit complex spatial organization that emerges because of the interplay of various cooperative and competitive interaction mechanisms. One strong competitive mechanism is contact-dependent neighbor killing enabled by the type VI secretion system. It has been previously shown that contact-dependent killing can result in bistability of bacterial mixtures so that only one strain survives and displaces the other. However, it remains unclear whether stable coexistence is possible in such mixtures. Using a population dynamics model for two interacting bacterial strains, we found that coexistence can be made possible by the interplay of contact-dependent killing and long-range growth inhibition, leading to the formation of various cellular patterns. These patterns emerge in a much broader parameter range than that required for the linear Turing-like instability, suggesting this may be a robust mechanism for pattern formation.
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Project description:The majority of ecological, industrial and medical impacts of bacteria result from diverse communities containing multiple species. This diversity presents a significant challenge as co-cultivation of multiple bacterial species frequently leads to species being outcompeted and, with this, the possibility to manipulate, evolve and improve bacterial communities is lost. Ecological theory predicts that a solution to this problem will be to grow species in structured environments, which reduces the likelihood of competitive exclusion. Here, we explored the ability of cultivation in a structured environment to facilitate coexistence, evolution, and adaptation in an industrially important community: Lactococcus lactis and Leuconostoc mesenteroides frequently used as dairy starter cultures. As commonly occurs, passaging of these two species together in a liquid culture model led to the loss of one species in 6 of 20 lineages (30%). By contrast, when we co-cultured the two species as biofilms on beads, a stable coexistence was observed in all lineages studied for over 100 generations. Moreover, we show that the co-culture drove evolution of new high-yield variants, which compared to the ancestor grew more slowly, yielded more cells and had enhanced capability of biofilm formation. Importantly, we also show that these high-yield biofilm strains did not evolve when each species was passaged in monoculture in the biofilm model. Therefore, both co-culture and the biofilm model were conditional for these high-yield strains to evolve. Our study underlines the power of ecological thinking-namely, the importance of structured environments for coexistence-to facilitate cultivation, evolution, and adaptation of industrially important bacterial communities.
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Project description:Streptococcus mutans is a biofilm-forming oral pathogen commonly associated with dental caries. Clinical studies have shown that S. mutans is often detected with Candida albicans in early childhood caries. Although the C. albicans presence has been shown to enhance bacterial accumulation in biofilms, the influence of S. mutans on fungal biology in this mixed-species relationship remains largely uncharacterized. Therefore, we aimed to investigate how the presence of S. mutans influences C. albicans biofilm development and coexistence. Using a newly established haploid biofilm model of C. albicans, we found that S. mutans augmented haploid C. albicans accumulation in mixed-species biofilms. Similarly, diploid C. albicans also showed enhanced biofilm formation in the presence of S. mutans. Surprisingly, the presence of S. mutans restored the biofilm-forming ability of C. albicans bcr1Δ mutant and bcr1Δ/Δ mutant, which is known to be severely defective in biofilm formation when grown as single species. Moreover, C. albicans hyphal growth factor HWP1 as well as ALS1 and ALS3, which are also involved in fungal biofilm formation, were upregulated in the presence of S. mutans. Subsequently, we found that S. mutans-derived glucosyltransferase B (GtfB) itself can promote C. albicans biofilm development. Interestingly, GtfB was able to increase the expression of HWP1, ALS1, and ALS3 genes in the C. albicans diploid wild-type SC5314 and bcr1Δ/Δ, leading to enhanced fungal biofilms. Hence, the present study demonstrates that a bacterial exoenzyme (GtfB) augments the C. albicans counterpart in mixed-species biofilms through a BCR1-independent mechanism. This novel finding may explain the mutualistic role of S. mutans and C. albicans in cariogenic biofilms.
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Project description:The emergence and spread of antibiotic resistance in bacterial pathogens are a global crisis. Because many bacterial infections are caused by pathogens that reside in biofilms, we sought to investigate how biofilms influence the evolution of antibiotic resistance. We hypothesize that the inherent spatial structure of biofilms facilitates the accumulation and persistence of spontaneously evolved antibiotic-resistant mutants. To test this, we tracked the frequency of mutants resistant to kanamycin and rifampicin in biofilm populations of Escherichia coli before, during, and after an antibiotic treatment regimen. Our results show that biofilms accumulate resistant mutants even in the absence of antibiotics. This resistance was found to be heritable and thus unlike the phenotypic plasticity of so-called "persister cells" that have been shown to occur in biofilms. Upon exposure to an antibiotic, resistant mutants swept to high frequency. Following the conclusion of treatment, these resistant mutants remained at unexpectedly high frequencies in the biofilms for over 45 days. In contrast, when samples from kanamycin-treated biofilms were used to found well-mixed liquid cultures and propagated by serial transfer, the frequency of resistant cells dramatically decreased as they were outcompeted by sensitive clones. These observations suggest that the emergence of antibiotic resistance through spontaneous mutations in spatially structured biofilms may significantly contribute to the emergence and persistence of mutants that are resistant to antibiotics used to treat bacterial infections.
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Project description:BackgroundContact-dependent inhibition (CDI) has been recently revealed as an intriguing but ubiquitous mechanism for bacterial competition in which a species injects toxins into its competitors through direct physical contact for growth suppression. Although the molecular and genetic aspects of CDI systems are being increasingly explored, a quantitative and systematic picture of how CDI systems benefit population competition and hence alter corresponding competition outcomes is not well elucidated.ResultsBy constructing a mathematical model for a population consisting of CDI+ and CDI- species, we have systematically investigated the dynamics and possible outcomes of population competition. In the well-mixed case, we found that the two species are mutually exclusive: Competition always results in extinction for one of the two species, with the winner determined by the tradeoff between the competitive benefit of the CDI+ species and its growth disadvantage from increased metabolic burden. Initial conditions in certain circumstances can also alter the outcome of competition. In the spatial case, in addition to exclusive extinction, coexistence and localized patterns may emerge from population competition. For spatial coexistence, population diffusion is also important in influencing the outcome. Using a set of illustrative examples, we further showed that our results hold true when the competition of the population is extended from one to two dimensional space.ConclusionsWe have revealed that the competition of a population with CDI can produce diverse patterns, including extinction, coexistence, and localized aggregation. The emergence, relative abundance, and characteristic features of these patterns are collectively determined by the competitive benefit of CDI and its growth disadvantage for a given rate of population diffusion. Thus, this study provides a systematic and statistical view of CDI-based bacterial population competition, expanding the spectrum of our knowledge about CDI systems and possibly facilitating new experimental tests for a deeper understanding of bacterial interactions.
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Project description:Myocardial infarction (MI) results in the generation of dead cells in the infarcted area. These cells are swiftly removed by phagocytes to minimize inflammation and limit expansion of the damaged area. However, the types of cells and molecules responsible for the engulfment of dead cells in the infarcted area remain largely unknown. In this study, we demonstrated that cardiac myofibroblasts, which execute tissue fibrosis by producing extracellular matrix proteins, efficiently engulf dead cells. Furthermore, we identified a population of cardiac myofibroblasts that appears in the heart after MI in humans and mice. We found that these cardiac myofibroblasts secrete milk fat globule-epidermal growth factor 8 (MFG-E8), which promotes apoptotic engulfment, and determined that serum response factor is important for MFG-E8 production in myofibroblasts. Following MFG-E8-mediated engulfment of apoptotic cells, myofibroblasts acquired antiinflammatory properties. MFG-E8 deficiency in mice led to the accumulation of unengulfed dead cells after MI, resulting in exacerbated inflammatory responses and a substantial decrease in survival. Moreover, MFG-E8 administration into infarcted hearts restored cardiac function and morphology. MFG-E8-producing myofibroblasts mainly originated from resident cardiac fibroblasts and cells that underwent endothelial-mesenchymal transition in the heart. Together, our results reveal previously unrecognized roles of myofibroblasts in regulating apoptotic engulfment and a fundamental importance of these cells in recovery from MI.
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