Black Queen evolution: the role of leakiness in structuring microbial communities

Morris, Jeffrey

doi:10.1016/j.tig.2015.05.004

Cited by 183 publications

(226 citation statements)

References 97 publications

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“…The model predicted that different NH 4 + excretion levels would establish a range of stable equilibria (Figure 6a). These distinct equilibria are likely all stabilized by negative frequency-dependent selection on E. coli (Morris, 2015), wherein the relative amount of NH 4 + available per E. coli cell, which determines E. coli fitness, decreases as the E. coli frequency increases. The level of NH 4 + exchange also influenced organic acid …”

Section: Resultsmentioning

confidence: 99%

Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients

et al. 2016

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Microbial interactions, including mutualistic nutrient exchange (cross-feeding), underpin the flow of energy and materials in all ecosystems. Metabolic exchanges are difficult to assess within natural systems. As such, the impact of exchange levels on ecosystem dynamics and function remains unclear. To assess how cross-feeding levels govern mutualism behavior, we developed a bacterial coculture amenable to both modeling and experimental manipulation. In this coculture, which resembles an anaerobic food web, fermentative Escherichia coli and photoheterotrophic Rhodopseudomonas palustris obligately cross-feed carbon (organic acids) and nitrogen (ammonium). This reciprocal exchange enforced immediate stable coexistence and coupled species growth. Genetic engineering of R. palustris to increase ammonium cross-feeding elicited increased reciprocal organic acid production from E. coli, resulting in culture acidification. Consequently, organic acid function shifted from that of a nutrient to an inhibitor, ultimately biasing species ratios and decreasing carbon transformation efficiency by the community; nonetheless, stable coexistence persisted at a new equilibrium. Thus, disrupting the symmetry of nutrient exchange can amplify alternative roles of an exchanged resource and thereby alter community function. These results have implications for our understanding of mutualistic interactions and the use of microbial consortia as biotechnology.

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Section: Resultsmentioning

confidence: 99%

Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients

et al. 2016

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“…Two mechanisms are conceivable how auxotrophs obtained the AAs they required for growth: metabolites might be exchanged among genotypes via diffusion through the cell-external environment [46–48] or, alternatively, in a contact-dependent manner [49, 50]. Recently it has been described that auxotrophic cells of E .…”

Section: Discussionmentioning

confidence: 99%

“…This race will most likely favor those loss-of-function mutants, which are fitter than other competing genotypes given the presence of a donor that can sufficiently compensate for their deficiencies. This ‘black-queen’-like process [46, 48] can then lead to coadaptations on both sides. Indeed, our observation that the AA-evolved auxotrophs grew significantly better when cocultured with the derived prototrophs than their evolutionary ancestor supports this interpretation (Fig 4A).…”

Section: Discussionmentioning

confidence: 99%

Experimental Evolution of Metabolic Dependency in Bacteria

2016

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Bacteria frequently lose biosynthetic genes, thus making them dependent on an environmental uptake of the corresponding metabolite. Despite the ubiquity of this ‘genome streamlining’, it is generally unclear whether the concomitant loss of biosynthetic functions is favored by natural selection or rather caused by random genetic drift. Here we demonstrate experimentally that a loss of metabolic functions is strongly selected for when the corresponding metabolites can be derived from the environment. Serially propagating replicate populations of the bacterium Escherichia coli in amino acid-containing environments revealed that auxotrophic genotypes rapidly evolved in less than 2,000 generations in almost all replicate populations. Moreover, auxotrophs also evolved in environments lacking amino acids–yet to a much lesser extent. Loss of these biosynthetic functions was due to mutations in both structural and regulatory genes. In competition experiments performed in the presence of amino acids, auxotrophic mutants gained a significant fitness advantage over the evolutionary ancestor, suggesting their emergence was selectively favored. Interestingly, auxotrophic mutants derived amino acids not only via an environmental uptake, but also by cross-feeding from coexisting strains. Our results show that adaptive fitness benefits can favor biosynthetic loss-of-function mutants and drive the establishment of intricate metabolic interactions within microbial communities.

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“…In fact, comparisons of different Acinetobacter genomes have shown that the presence of genes involving siderophore biosynthesis is predictive of high or low virulence [5]. Consistently, in bacteria including Acinetobacter baumannii , siderophores were shown as necessary components for the development of surface attachment and extracellular polysaccharide synthesis (termed biofilm formation) [6–8] and the establishment of mutually-beneficial, iron-sufficient microbial communities [9]. Given that siderophores are involved in biofilm formation which promotes antibiotic resistance [10, 11], targeting siderophores by blocking siderophore synthesis or function provides a promising alternative antimicrobial approach.…”

Section: Siderophores: Important Virulence Factors and Promising Molementioning

confidence: 99%

Siderophores in Iron Metabolism: From Mechanism to Therapy Potential

Wilson

Bogdan

Miyazawa

et al. 2016

Trends in Molecular Medicine

356

319

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Iron is an essential nutrient for life. During infection, a fierce battle of iron acquisition occurs between the host and bacterial pathogens. Bacteria acquire iron by secreting siderophores, small ferric iron binding molecules. In response, host immune cells secrete lipocalin 2 (also known as siderocalin), a siderophore-binding protein, to prevent bacterial reuptake of iron-loaded siderophores. To counter this threat, some bacteria can produce lipocalin 2-resistant siderophores. This review discusses the recently described molecular mechanisms of siderophore iron trafficking between host and bacteria, highlighting the therapeutic potential of exploiting pathogen siderophore machinery for the treatment of antibiotic-resistant bacterial infections. As the latter reflect a persistent problem in hospital settings, siderophore-targeting or siderophore-based compounds represent a promising avenue to combat such infections.

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Black Queen evolution: the role of leakiness in structuring microbial communities

Cited by 183 publications

References 97 publications

Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients

Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients

Experimental Evolution of Metabolic Dependency in Bacteria

Siderophores in Iron Metabolism: From Mechanism to Therapy Potential

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