The evolutionary ecology of interspecific microbial public-goods

Mine waste is a major problem worldwide, having detrimental effects on human health as well as the environment. There is a pressing need to develop long-term sustainable remediation strategies. Microbes play an important role in geochemical processes and their vast metabolic diversity may aid in the clean up of mine-degraded soils. Detoxification in microbial communities not only depends on individual behaviour, but on the collective action of different species. However, our knowledge of how different microbial species interact with one another to detoxify metals in polluted soils is limited. My overarching aim is to maximise microbial synergism in their efforts to detoxify environments and, more generally, to use evolutionary ecology theory to solve 'real world' problems.

Cooperation is common in bacteria, and has been well documented within individual species, where some strains produce costly compounds that are used by neighbouring cells (i.e. public-goods). Most of our understanding of microbial public-goods comes from work on within-species interactions, yet public-goods often simultaneously benefit other species. Key examples include the extracellular break down of antibiotics and environmental pollutants. Cooperation therefore has far-reaching consequences for human health, agriculture and ecosystem functioning. However, we currently have little understanding of the ecological constraints driving the evolution and quantity of community-wide public-goods production. Key drivers of within-species cooperation are: (1) spatial structure, resulting in predominantly localised interactions, (2) resource supply, which reduces marginal costs and (3) the need for multiple public goods, which provides opportunities for division of labour. These variables are likely to affect community-wide public goods differently to how they affect intra-specific public goods, requiring the need for novel theoretical and experimental studies.

I will develop novel theory to identify how key variables simultaneously affect cooperation within and between species. I will then test the theoretical predications in synthetic microbial communities, using the empirical results to refine theory. I will focus in on a ubiquitous social trait - the production of metal-detoxifying siderophores. Siderophores are perhaps best known for their function as iron-carriers, but these extracellular molecules can also bind to toxic metals and prevent them from being taking up and killing bacterial cells. This opens up the possibility of between-species cooperation but also exploitation, where species use other species' siderophores without paying their fair share. These controlled experiments allow me to tease apart ecological and evolutionary processes, and identify the molecular mechanisms underpinning changes in siderophore production. I will then apply this knowledge to the remediation of natural environments.

During the second phase of my research program, I will build on my results from phase one to increase our understanding of the role of microbial siderophores in driving plant-microbe interactions. Evidence is mounting that microbe-plant feedbacks are ubiquitous and a crucial determinant of their combined functioning. For example, plants and microbes produce signals that affect each other's behaviour, often to mutual benefit. However, we have little understanding of how these interactions are affected by cooperation and conflict within the interacting microbial communities. I will first test whether siderophore production is enhanced as a result of increased resource supply and structure in the plant root system and how siderophore-based cooperation between detoxifying microbes alters plant-microbe feedbacks, using both synthetic and natural soil communities.