Stability of Cross-Feeding Polymorphisms in Microbial Communities

Gudelj, Ivana; Kinnersley, Margie; Rashkov, Peter; Schmidt, Karen; Rosenzweig, Frank

doi:10.1371/journal.pcbi.1005269

Cited by 38 publications

(68 citation statements)

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“…also suggest, the more similar the metabolism is between cross‐feeding strains, the more likely it is that nutrient addition will shift a mutualism to a negative interaction. Consistent with this idea, mathematical predictions suggest that minimizing competition is critical for stabilizing cross‐feeding interactions (Doebeli, ; Pfeiffer and Bonhoeffer, ; Gudelj et al ., ; McCully et al ., ). It will be interesting to examine whether stable cross‐feeding interactions in natural systems are more common between species with smaller degrees of niche overlap.…”

Section: Discussionmentioning

confidence: 99%

A shared limiting resource leads to competitive exclusion in a cross‐feeding system

Hammarlund

Chacón

Harcombe

2019

Environmental Microbiology

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Summary Species interactions and coexistence are often dependent upon environmental conditions. When two cross-feeding bacteria exchange essential nutrients, the addition of a cross-fed nutrient to the environment can release one species from its dependence on the other. Previous studies suggest that continued coexistence depends on relative growth rates: coexistence is maintained if the slower-growing species is released from its dependence on the other, but if the faster-growing species is released, the slower-growing species will be lost (a hypothesis that we call “feed the faster grower” or FFG). Using invasion-from-rare experiments with two reciprocally cross-feeding bacteria, genome-scale metabolic modeling, and classical ecological models, we explored the potential for coexistence when one cross-feeder became independent. We found that whether nutrient addition shifted an interaction from mutualism to commensalism or parasitism depended on whether the nutrient that limited total growth was required by one or both species. Parasitism resulted when both species required the growth-limiting resource. Importantly, coexistence was only lost when the interaction became parasitism, and the obligate species had a slower growth rate. Under these restricted conditions, the FFG hypothesis applied. Our results contribute to a mechanistic understanding of how resources can be manipulated to alter interactions and coexistence in microbial communities.

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Section: Discussionmentioning

confidence: 99%

A shared limiting resource leads to competitive exclusion in a cross‐feeding system

Hammarlund

Chacón

Harcombe

2019

Environmental Microbiology

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“…5). While coexistence in natural and synthetic ecosystems has been studied in previous work [30,31,33], and is an obvious prerequisite for the possibility of increasing productivity by a consortium, the observation that this dependency works in both directions, in that the production of a heterologous protein affects coexistence as well, is a novel finding of this study. In particular, the analysis of the model shows that the coexistence region is shifted towards lower dilution rates (Fig.…”

Section: Discussionmentioning

confidence: 85%

“…The synthetic consortium considered here consists of two E. coli strains, one growing on glucose and producing the heterologous protein, and the other preferentially growing on acetate and thus removing this growth-inhibitory by-product from the environment [20]. While the overall structure of the model is similar to other population-based models of synthetic mutualistic consortia [28][29][30][31][32][33], it also differs on key points from previous work in order to account for regulatory mechanisms specific to E. coli. We here explain the model for the producer strain in detail and then appropriately modify the model for the cleaner in The consortium consists of two bacterial species.…”

Section: Resultsmentioning

confidence: 99%

“…2). Like in other work on the mathematical modeling of community dynamics [28][29][30][31][32][33], we have developed coarsegrained models of the physiology of the individual species in the consortium, which requires making stark simplying assumptions (see [24,27] for other perspectives, based on genome-wide flux balance models). Despite the simplifications, however, a critical requirement to assess the potential for productivity gains is the ability of the model to qualitatively and quantitatively reproduce nutrient production and consumption patterns, as well as to predict the growth rates of individual species.…”

Section: Discussionmentioning

confidence: 99%

“…The models we develop differ in two main respects from existing coarse-grained models of similarly structured communities [28][29][30][31][32][33]. First, we take into account a range of mechanisms controlling the growth phenotypes of the E. coli strains constituting our consortium, with the aim of obtaining quantitatively predictive models.…”

Section: Introductionmentioning

confidence: 99%

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Enhanced production of heterologous proteins by a synthetic microbial community: Conditions and trade-offs

Mauri

Gouzé

Jong

et al. 2020

Preprint

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AbstractSynthetic microbial consortia have been increasingly utilized in biotechnology and experimental evidence shows that suitably engineered consortia can outperform individual species in the synthesis of valuable products. Despite significant achievements, though, a quantitative understanding of the conditions that make this possible, and of the trade-offs due to the concurrent growth of multiple species, is still limited. In this work, we contribute to filling this gap by the investigation of a known prototypical synthetic consortium. A first E. coli strain, producing a heterologous protein, is sided by a second E. coli strain engineered to scavenge toxic byproducts, thus favoring the growth of the producer at the expense of diverting part of the resources to the growth of the cleaner. The simplicity of the consortium is ideal to perform an in depth-analysis and draw conclusions of more general interest. We develop a coarse-grained mathematical model that quantitatively accounts for literature data from different key growth phenotypes. Based on this, assuming growth in chemostat, we first investigate the conditions enabling stable coexistence of both strains and the effect of the metabolic load due to heterologous protein production. In these conditions, we establish when and to what extent the consortium outperforms the producer alone in terms of productivity. Finally, we show in chemostat as well as in a fed-batch scenario that gain in productivity comes at the price of a reduced yield, reflecting at the level of the consortium resource allocation trade-offs that are well-known for individual species.

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Geometric analysis of a model for cross‐feeding in the chemostat

Rashkov

2018

Math Methods in App Sciences

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A model for competition between bacterial strains in a chemostat is studied using a model reduction argument and phase portrait analysis for the specific case of trophic chain. The first strain feeds on glucose but secretes a metabolic intermediate (acetate), which the second strain consumes. However, the metabolic intermediate imposes a cost to growth to both strains. The geometric and asymptotic analysis of the reduced model allows a rigourous treatment of the role of this assumption in the emergence of coexistence (cross-feeding) equilibria. Conditions for non-existence of cross-feeding equilibria are given for certain parameter ranges. In the case of trophic chains, existence of cross-feeding equilibria does not rely only on the presence of the acetate specialist scavenging for the intermediate metabolite inside the resource-limited chemostat environment. The glucose specialist must, in addition, possess a certain degree of tolerance to the metabolic intermediate. Relaxing the assumption of the cost of growth helps establish a cross-feeding equilibrium.KEYWORDS bifurcation analysis, chemostat, cross-feeding INTRODUCTIONMetabolic interactions affect the function and stability of microbial communities and obtaining understanding on them is crucial in many biological applications. 1 When multiple microbial strains share a single limiting resource in a well-stirred chemostat, the outcome is competitive exclusion where at most one strain could be stably sustained over time. [2][3][4][5][6] However, when one strain consumes metabolites produced by the other (via cross-feeding), stable coexistence of both strains may be possible. 1,7,8 The study 9 shows that locally asymptotically stable coexistence between 2 strains of Escherichia coli occurs because of cross-feeding for different ranges of the glucose input and appropriate initial population densities.The mathematical model proposed by Gudelj et al 9 builds upon 10 and describes the dynamics of competition between the strains, which metabolise glucose in a 2-step process: glycolysis and tricarboxylic acid (TCA) cycle. In the first step, the bacterial cell partially converts the glucose to a metabolic intermediate (acetate), and in the second step it, either fully consumes the intermediate or releases it in the environment. The excreted metabolic intermediate creates additional resource niches, where other strains can grow, and the model 9 bypasses the assumptions of the competitive exclusion principle. The models 9,10 assume both strains feed on either resource but differ in the respective uptake kinetics as observed by Rosenzweig et al. 8 Thus, the strain with higher affinity for glucose shall be called glucose specialist, and the second strain with higher affinity for acetate acetate specialist.As a possible biological mechanism behind the observed outcome, 8 mentions changes in glucose uptake kinetics by the glucose specialist resulting from scavenging for the limiting resource. However, the upregulated glucose fermenta-Math Meth Appl Sci. 2018;41:8765-8783.wi...

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Stability of Cross-Feeding Polymorphisms in Microbial Communities

Cited by 38 publications

References 56 publications

A shared limiting resource leads to competitive exclusion in a cross‐feeding system

A shared limiting resource leads to competitive exclusion in a cross‐feeding system

Enhanced production of heterologous proteins by a synthetic microbial community: Conditions and trade-offs

Geometric analysis of a model for cross‐feeding in the chemostat

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