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Bacterial siderophores in community and host interactions

Nature Reviews Microbiology volume 18, pages 152–163 (2020)Cite this article

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Abstract

Iron is an essential trace element for most organisms. A common way for bacteria to acquire this nutrient is through the secretion of siderophores, which are secondary metabolites that scavenge iron from environmental stocks and deliver it to cells via specific receptors. While there has been tremendous interest in understanding the molecular basis of siderophore synthesis, uptake and regulation, questions about the ecological and evolutionary consequences of siderophore secretion have only recently received increasing attention. In this Review, we outline how eco-evolutionary questions can complement the mechanistic perspective and help to obtain a more integrated view of siderophores. In particular, we explain how secreted diffusible siderophores can affect other community members, leading to cooperative, exploitative and competitive interactions between individuals. These social interactions in turn can spur co-evolutionary arms races between strains and species, lead to ecological dependencies between them and potentially contribute to the formation of stable communities. In brief, this Review shows that siderophores are much more than just iron carriers: they are important mediators of interactions between members of microbial assemblies and the eukaryotic hosts they inhabit.

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Fig. 1: Representative examples of the four main chemical classes of siderophores.
Fig. 2: Comparison of siderophore-dependent and surface-dependent iron-uptake systems.
Fig. 3: Siderophores can synergistically increase iron uptake when bacteria live in groups.
Fig. 4: Siderophore-mediated social interactions.
Fig. 5: Siderophores induce eco-evolutionary dynamics in bacterial communities.
Fig. 6: Siderophores and their effects on hosts.

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Acknowledgements

This work was funded by the European Research Council under grant agreement no. 681295 and the Swiss National Science Foundation under grant no. 31003A_182499 (both to R. K.), the German Science Foundation under grant no. KR 5017/2-1 (to J. K.) and a University Research Priority Program (Evolution in Action) grant (to Ö. Ö.).

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    Jos Kramer, Özhan Özkaya & Rolf Kümmerli

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Glossary

Siderophores

Secondary metabolites with high affinity and specificity for iron that function as organic ligands, serve the purpose of iron acquisition and are regulated in response to the producer’s need for iron.

Biofilms

Aggregates of microorganisms that are embedded within a self-produced matrix of extracellular polymeric substances and that adhere to each other and/or a surface.

Cooperation

A social behaviour which provides a benefit to another individual and which has evolved and/or is currently maintained (at least partly) because of its beneficial effect on the recipient.

Pseudomonas aeruginosa

A metabolically versatile, ubiquitous, rod-shaped, Gram-negative bacterium that can opportunistically infect plants, animals and humans and is known for its high intrinsic resistance to antibiotics.

Public goods

Costly resources that benefit not only the producer but also other members of the population or local community.

Tragedy of the commons

A situation in which cooperation would be beneficial in the long term but breaks down because individuals selfishly pursue their own short-term interests.

Negative frequency-dependent selection

An evolutionary process by which the relative fitness of a phenotype is high when it occurs at low frequency in the population but decreases as it becomes more common relative to other phenotypes.

Cheating

Exploitation of a cooperative behaviour by an individual that does not cooperate (or cooperates less than its fair share), whereby the cheating individual reaps the benefits of cooperation at the expense of the cooperating individual.

Competition

A situation that arises when two or more individuals of the same species or different species strive for the same limited resource, resulting in immediate costs for all individuals involved.

Horizontal gene transfer

The transfer of genetic material from one individual to another individual (of the same species or a different species) that does not involve the vertical transmission of DNA typical of cell division and reproduction.

Co-evolutionary arms races

Evolutionary tug of war between competing strains or species, whereby adaptations in one party select for counteradaptations in the other party.

Non-transitive population dynamics

Population dynamics arising from non-hierarchical circular competitive relationships between species, in which each species is both superior and inferior to different community members, with no overall winner existing in the population.

Metallophores

Secondary metabolites with high affinity and specificity for a given metal. They function as an organic ligand, serve the purpose of acquiring the metal in question and are regulated in response to metal limitation.

Division of labour

The division of a task that occurs when cooperating individuals specialize to carry out specific subtasks.

Cross-feeding

A nutritional interdependence between different strains or species in which each species feeds on the metabolic products released by the other species.

Virulence

The damage caused to the host by a parasite or pathogen, measured as the decrease in host fitness.

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Kramer, J., Özkaya, Ö. & Kümmerli, R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol 18, 152–163 (2020). https://doi.org/10.1038/s41579-019-0284-4

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