Ecological selection of siderophore-producing microbial taxa in response to heavy metal contamination

Abstract

Some microbial public goods can provide both individual and community-wide benefits, and are open to exploitation by non-producing species. One such example is the production of metal-detoxifying siderophores. Here, we investigate whether heavy metals select for increased siderophore production in natural microbial communities, or whether exploitation of this detoxifying effect reduces siderophore production. We show that the proportion of siderophore-producing taxa increases along a natural heavy metal gradient. A causal link between metal contamination and siderophore production was subsequently demonstrated in a microcosm experiment in compost, in which we observed changes in community composition towards taxa that produce relatively more siderophores following copper contamination. We confirmed the selective benefit of siderophores by showing that taxa producing large amount of siderophores suffered less growth inhibition in toxic copper. Our results suggest that ecological selection will favour siderophore-mediated decontamination, with important consequences for potential remediation strategies.AuthorshipEH, SOB, AL, DJH, EvV, AB conceived and designed the experiment. DJH provided new perspectives. EH, SOB, FB, AL collected the data. EH, FB, NT, DJH carried out the data analyses. EH & AB wrote the first draft of the manuscript, and all authors contributed substantially to revisions.Data accessibility:Upon acceptance, data presented in the manuscript will be made available on Dryad.

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

“…This was recently demonstrated in vitro, where P. aeruginosa cheat growth was increased by the addition of purified siderophores from different species (Hesse et al. ). However, it is unclear to which extent siderophores act as public goods in natural, metal‐contaminated environments: recent work reported ecological selection for increased siderophore production in contaminated soil and compost, suggesting fitness benefits of siderophores outweighed any cost associated with exploitation (Hesse et al.…”

“…The NMC is pictured as yellow or purple to illustrate the variation in siderophore production among members of the natural community (Hesse et al. ). This design was performed in the presence and absence of CuSO 4 .…”

“…However, it is unclear to which extent siderophores act as public goods in natural, metal‐contaminated environments: recent work reported ecological selection for increased siderophore production in contaminated soil and compost, suggesting fitness benefits of siderophores outweighed any cost associated with exploitation (Hesse et al. ).…”

“…Note that previous work has established that siderophores can act as metal decontaminating interspecific public goods in vitro (Hesse et al. ), but it is unclear if this is the case in natural environments such as compost or soil, where siderophores are known to be expressed (Marcschner and Crowley ). As a corollary of this prediction, being embedded within a microbial community will then reduce the importance of relatedness that is, the extent to which conspecific producers and nonproducers interact with each other—in determining selection for siderophore production in contaminated compost.…”

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

“…; Hesse et al. ), and drive community dynamics by supressing the growth of competitors (Butaitė et al. ) or benefiting close relatives through cooperative molecule sharing (Griffin et al.…”