Social evolution of microbial heavy metal bioremediation

Human-imposed heavy metal contamination of soils and groundwater is a major problem both for natural ecosystems and the development of brown-field sites. Conventional physico-chemical methods of heavy metal removal from contaminated sites are too expensive to be carried out on larger scales, and may themselves have adverse effects on soil structure and function. A particularly promising and cost-effective approach is phytoremediation - the use of heavy-metal tolerant plants to absorb the heavy metals. However, the success of phytoremediation is dependent on the microbial community producing extracellular molecules, siderophores. While the primary role of siderophores is to scavenge iron, they also bind toxic heavy metals. Heavy metals are more readily taken up by plants when bound to microbial siderophores, and siderophore production in contaminated sites detoxifies the environment for the microbial community, which in turn promotes increased plant growth. Maximising microbial siderophore production will therefore greatly increase the success of phytoremediation.
Unfortunately, evolution does not always work in our favour, and both theory and our test-tube experiments suggest that microbes rapidly evolve to make less siderophore in metal-contaminated sites. This is because siderophore production is metabolically costly to the individual cell, but provides a benefit to all individuals in the environment through heavy metal decontamination. As such, non-siderophore producing “cheats” will have a fitness advantage over siderophore producers, at the expense of the community as a whole. While the problem could in principle be solved by the continual addition of high siderophore-producing bacteria, this is not practical outside of the lab.
There is a solution: change the environment so that siderophore production is directly beneficial to the producing individuals, hence preventing cheats from evolving. Siderophores are directly beneficial to individual producers when iron is insoluble, and iron is insoluble in non-acidic environments. Fortunately, soil acidity can be easily and cheaply reduced by the addition of lime.
We will determine if our in vitro findings, that heavy metal contamination results in the evolution of siderophore cheating, also applies in natural populations by measuring microbial siderophore production in heavy-metal contaminated (through mining) or uncontaminated sites across Cornwall. We will then determine causal links between metal contamination, acidity and the evolution of siderophore production by evolving natural soil communities in real-time under controlled conditions. Finally, we will determine how these evolved communities that differ in siderophore production affect the ability of a metal hyper-accumulating plant to suck up the heavy metal contaminants. To achieve our goals, we have assembled a highly interdisciplinary team specializing in high throughput genome sequencing, microbial experimental evolution, physical chemistry and mathematical modeling.
The study has the potential to pave the way for highly effective phytoremediation of heavy metals. Moreover, the study will be the first application of the rapidly expanding field of microbial social evolution to a real problem; and the first studied example of social evolution within the context of whole communities, rather than simply within species.

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