Public goods exploitation is reduced in species-rich microbial communities

Abstract

Intraspecific public goods are commonly shared within microbial populations, where the benefits of public goods are largely limited to closely related conspecifics. One example is the production of iron-scavenging siderophores that deliver iron to cells via specific cell envelope receptor and transport systems. Intraspecific social exploitation of siderophore producers is common, since non-producers avoid the costs of production but retain the cell envelope machinery for siderophore uptake. However, little is known about how interactions between species (i.e. interspecific interactions) can shape intraspecific public goods exploitation. Here, we predicted that strong competition for iron between species in diverse communities will increase costs of siderophore cooperation, and hence select for increased intraspecific exploitation. We examined how increasing microbial community species diversity shapes intraspecific social dynamics by monitoring the growth of siderophore producers and non-producers of the plant-growth promoting bacterium Pseudomonas fluorescens, embedded within tree-hole microbial communities ranging from 2-15 species. We find, contrary to our prediction, that siderophore exploitation is reduced in high diversity communities, driven by increased likelihood of encountering key species that reduce the growth of siderophore non-producing (but not producing) strains of P. fluorescens. Our results suggest that maintaining a healthy soil microbiota could contribute to the maintenance of siderophore production in natural communities.

Ecological histories determine the success of social exploitation

“…For example, environmental toxins such as antibiotics (Vasse et al 2017) or heavy metals (O'Brien et al 2014) can benefit cheaters, while oxidative stress (García-Contreras et al 2015) and viscosity (Kümmerli et al 2009a) can benefit cooperators. High diversity (O'Brien et al 2022), competitors (Harrison et al 2008), or predators (Friman et al 2013) within communities can also benefit cooperators. In some cases, phage presence benefits cooperators (Morgan et al 2012;Saucedo-Mora et al 2017), but in others it benefits cheaters (O'Brien et al 2019;Vasse et al 2015).…”

“…2009a) can benefit cooperators. High diversity (O’Brien et al . 2022), competitors (Harrison et al .…”