Habitat structure and the evolution of diffusible siderophores in bacteria

Kümmerli, Rolf; Schiessl, Konstanze T.; Waldvogel, Tuija; McNeill, Kristopher; Ackermann, Martin

doi:10.1111/ele.12371

Cited by 104 publications

(101 citation statements)

References 48 publications

(103 reference statements)

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“…13). In many cases, a likely important factor enabling coexistence is spatial structure (62)(63)(64), whereby spatial segregation of nonproducers and producers limits the exploitative potential of the former. In one of the few studies investigating interactions between antibiotics and social behaviors in bacteria, Diard et al (14) assessed the in vivo impact of ciprofloxacin on competition between virulent cooperative Salmonella enterica serovar Typhimurium and avirulent defectors.…”

Section: Discussionmentioning

confidence: 99%

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Vasse

Noble

Akhmetzhanov

et al. 2017

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

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Cheats are a pervasive threat to public goods production in natural and human communities, as they benefit from the commons without contributing to it. Although ecological antagonisms such as predation, parasitism, competition, and abiotic environmental stress play key roles in shaping population biology, it is unknown how such stresses generally affect the ability of cheats to undermine cooperation. We used theory and experiments to address this question in the pathogenic bacterium, Pseudomonas aeruginosa. Although public goods producers were selected against in all populations, our competition experiments showed that antibiotics significantly increased the advantage of nonproducers. Moreover, the dominance of nonproducers in mixed cultures was associated with higher resistance to antibiotics than in either monoculture. Mathematical modeling indicates that accentuated costs to producer phenotypes underlie the observed patterns. Mathematical analysis further shows how these patterns should generalize to other taxa with public goods behaviors. Our findings suggest that explaining the maintenance of cooperative public goods behaviors in certain natural systems will be more challenging than previously thought. Our results also have specific implications for the control of pathogenic bacteria using antibiotics and for understanding natural bacterial ecosystems, where subinhibitory concentrations of antimicrobials frequently occur.evolution | cooperation | antibiotics | social behavior | resistance P ublic goods production is a characteristic of a diverse range of taxa, from microbes to humans (1-3). Explaining the persistence of this costly behavior is challenging, because cheats can exploit the commons without contributing. Kin selection theory has proven to be a successful framework for addressing this question, with the central prediction that cooperation is favored by sufficient benefits to, and positive assortment between, cooperators (4-8). For example, recent study in experimental bacterial populations has elucidated mechanisms such as assortment emerging from limited or budding dispersal (9, 10) and kin discrimination (11, 12) that are consistent with kin selection fostering cooperative behaviors (e.g., refs. 8 and 13). However, despite this accumulating consensus, little is known about how social populations respond to differences and variation in abiotic and biotic components of their environment. In particular, it is unclear how ecological antagonisms affect the ability of cheats to invade cooperator communities.Cooperation can be affected by stress directly through differential selection on cooperative phenotypes (14, 15), or by inducing specific plastic behaviors (16-22), especially when cooperation leads to increased stress resistance. However, in the absence of a direct benefit of the cooperative behavior against stress, the ecological and evolutionary outcomes of the interactions between nondefensive public goods and stress responses are less clear and are potentially complex. Cooperation may be infl...

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Section: Discussionmentioning

confidence: 99%

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Vasse

Noble

Akhmetzhanov

et al. 2017

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

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“…Although it has long been suspected that many siderophores might remain cell associated after secretion (25,(55)(56)(57), evidence for this notion is limited and restricted to a few bacterial species. Furthermore, aside from the few studies on amphiphilic siderophores and pyoverdine, the mechanisms for privatization appear to be largely unexplored (23,24,26).…”

Section: Discussionmentioning

confidence: 99%

“…Evidence indicates that adherence of FeEnt to the surface of E. coli is almost entirely mediated by FepA (58), but the mechanism for apo-Ent adherence is unclear, as studies typically measure adsorbance and transport of radiolabeled iron-siderophore complexes into cells, not aposiderophores (59). Due to the hydrophobicity of apo-Ent, it is possible that it remains associated with the cell surface after secretion (25,56). We have not addressed the mechanism of Ent privatization, but we have found that iron chelated with transferrin supports growth of E. coli only when cells are at sufficient population densities or if exogenous enterochelin is added.…”

Section: Discussionmentioning

confidence: 99%

“…Some bacteria have also evolved mechanisms that appear to prevent or minimize siderophore freeloading, including maintaining variability in structure of siderophore-receptor pairs (diversifying selection) (21,22) and privatizing siderophores through high hydrophobicity or association with membrane-bound receptors (23)(24)(25)(26). We are interested in siderophore maintenance through privatization, for which there is little direct evidence in microbes (24).…”

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confidence: 99%

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Sociality in Escherichia coli: Enterochelin Is a Private Good at Low Cell Density and Can Be Shared at High Cell Density

Scholz

Greenberg

2015

J. Bacteriol.

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Many bacteria produce secreted iron chelators called siderophores, which can be shared among cells with specific siderophore uptake systems regardless of whether the cell produces siderophores. Sharing secreted products allows freeloading, where individuals use resources without bearing the cost of production. Here we show that the Escherichia coli siderophore enterochelin is not evenly shared between producers and nonproducers. Wild-type Escherichia coli grows well in low-iron minimal medium, and an isogenic enterochelin synthesis mutant (⌬entF) grows very poorly. The enterochelin mutant grows well in low-iron medium supplemented with enterochelin. At high cell densities the ⌬entF mutant can compete equally with the wild type in lowiron medium. At low cell densities the ⌬entF mutant cannot compete. Furthermore, the growth rate of the wild type is unaffected by cell density. The wild type grows well in low-iron medium even at very low starting densities. Our experiments support a model where at least some enterochelin remains associated with the cells that produce it, and the cell-associated enterochelin enables iron acquisition even at very low cell density. Enterochelin that is not retained by producing cells at low density is lost to dilution. At high cell densities, cell-free enterochelin can accumulate and be shared by all cells in the group. Partial privatization is a solution to the problem of iron acquisition in low-iron, low-cell-density habitats. Cell-free enterochelin allows for iron scavenging at a distance at higher population densities. Our findings shed light on the conditions under which freeloaders might benefit from enterochelin uptake systems. IMPORTANCESociality in microbes has become a topic of great interest. One facet of sociality is the sharing of secreted products, such as the iron-scavenging siderophores. We present evidence that the Escherichia coli siderophore enterochelin is relatively inexpensive to produce and is partially privatized such that it can be efficiently shared only at high producer cell densities. At low cell densities, cell-free enterochelin is scarce and only enterochelin producers are able to grow in low-iron medium. Because freely shared products can be exploited by freeloaders, this partial privatization may help explain how enterochelin production is stabilized in E. coli and may provide insight into when enterochelin is available for freeloaders. Iron is an essential nutrient for the vast majority of bacteria (1, 2). However, under aerobic conditions at neutral pH, iron is found predominantly in insoluble Fe 3ϩ compounds, resulting in extremely low iron concentrations in water (about 10 Ϫ18 M) (3). Within a host, available iron is also limited, as many host organisms produce iron-binding molecules, which sequester iron away from bacteria (4). Thus, bacteria have evolved a variety of mechanisms to acquire this resource. One mechanism is to secrete molecules, called siderophores, that bind and solubilize extracellular iron. Different bacteria produce differ...

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“…For example, many bacteria engage in mutualistic behaviors such as siderophore production, which assists the whole bacterial population in iron-scavenging behaviors [28] (although note that this behavior may decline with the spatial scale of competition [29]). Assistance provided by a coinfection may also be a byproduct of other processes.…”

Section: Resource Modulationmentioning

confidence: 99%

The potential impact of coinfection on antimicrobial chemotherapy and drug resistance

Birger

Kouyos

Cohen

et al. 2015

Trends in Microbiology

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Across a range of pathogens, resistance to chemotherapy is a growing problem in both public health and animal health. Despite the ubiquity of coinfection, and its potential effects on within-host biology, the role played by coinfecting pathogens on the evolution of resistance and efficacy of antimicrobial chemotherapy is rarely considered. In this review, we provide an overview of the mechanisms of interaction of coinfecting pathogens, ranging from immune modulation and resource modulation, to drug interactions. We discuss their potential implications for the evolution of resistance, providing evidence in the rare cases where it is available. Overall, our review indicates that the impact of coinfection has the potential to be considerable, suggesting that this should be taken into account when designing antimicrobial drug treatments.

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Habitat structure and the evolution of diffusible siderophores in bacteria

Cited by 104 publications

References 48 publications

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

Sociality in Escherichia coli: Enterochelin Is a Private Good at Low Cell Density and Can Be Shared at High Cell Density

The potential impact of coinfection on antimicrobial chemotherapy and drug resistance

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