The evolution of siderophore production as a competitive trait

Abstract

Microbes have the potential to be highly cooperative organisms. The archetype of microbial cooperation is often considered to be the secretion of siderophores, molecules scavenging iron, where cooperation is threatened by "cheater" genotypes that use siderophores without making them. Here, we show that this view neglects a key piece of biology: siderophores are imported by specific receptors that constrain their use by competing strains. We study the effect of this specificity in an ecoevolutionary model, in which we vary siderophore sharing among strains, and compare fully shared siderophores with private siderophores. We show that privatizing siderophores fundamentally alters their evolution. Rather than a canonical cooperative good, siderophores become a competitive trait used to pillage iron from other strains. We also study the physiological regulation of siderophores using in silico long-term evolution. Although shared siderophores evolve to be downregulated in the presence of a competitor, as expected for a cooperative trait, privatized siderophores evolve to be upregulated. We evaluate these predictions using published experimental work, which suggests that some siderophores are upregulated in response to competition akin to competitive traits like antibiotics. Although siderophores can act as a cooperative good for single genotypes, we argue that their role in competition is fundamental to understanding their biology.

Modified chrome azurol S method for detection and estimation of siderophores having affinity for metal ions other than iron

“…) to coordinate with the ferric ion (Neilands 1981;Neilands 1995;Miethke and Marahiel 2007;Sonawane et al 2016;Wani et al 2016;Niehus et al 2017;Ellermann and Arthur 2017). However, microorganisms also need metal ions other than Fe 3+ and in order to chelate these metal ions, they produce various other types of siderophores.…”

No effect of intraspecific relatedness on public goods cooperation in a complex community

“…; De Gasperin and Kilner ; Niehus et al. ). For example, the presence of other species may affect population structure of a focal species (Mitri et al.…”

Receptor uptake arrays for vitamin B12, siderophores, and glycans shape bacterial communities

“…; Degnan, Taga, et al. ; Niehus et al., ). Continual selection for novel private variants could diversify corrinoids.…”

“…Diversity of form may be influenced primarily by extracellular scavenging in different physical and competitive environments (Kümmerli, Schiessl, Waldvogel, McNeill, & Ackermann, ). Specificity of cellular uptake in relation to competition may favor differentiation into private types and increased diversity ((Niehus et al., , see earlier section Why are there different types of corrinoid ? ).…”

“…Iron often sets a limiting resource for microbial growth. Thus, competitive and cooperative processes over siderophore uptake shape bacterial community dynamics (Chakraborty, Braun, Hantke, & Cornelis, ; Niehus, Picot, Oliveira, Mitri, & Foster, ; West, Diggle, Buckling, Gardner, & Griffin, ). Individual bacteria may secrete more than one type of siderophore, or none at all.…”