Reconciling concepts of black queen and tragedy of the commons in simulated bulk soil and rhizosphere prokaryote communities.

Abstract

The Black Queen hypothesis describes the evolutionary strategy to lose costly functions in favour of improving growth efficiency. This results in mutants (cheaters) becoming obligately dependent upon a provider (black queen) to produce a necessary resource. Previous analyses demonstrate black queens and cheaters reach a state of equilibrium in pair-wise systems. However, in complex communities, accumulation of cheaters likely poses a serious burden on shared resources. This should result in a Tragedy of the Commons (ToC), whereby over-utilisation of public resources risks making them growth-limiting. With a collection of differential equations, microbial communities composed of twenty prokaryote ‘species’ either from rhizosphere, characterised by abundant carbon and energy sources, or bulk soil, with limited carbon and energy supply, were simulated. Functional trait groups differed based on combinations of cellulase and amino acid production, growth and resource uptake. Randomly generated communities were thus composed of species that acted as cellulolytic prototrophic black queens, groups that were either cellulolytic or prototrophic, or non-cellulolytic auxotrophic cheaters. Groups could evolve to lose functions over time. Biomass production and biodiversity were tracked in 8,000 Monte Carlo simulations over 500 generations. Bulk soil favoured oligotrophic co-operative communities where biodiversity was positively associated with growth. Rhizosphere favoured copiotrophic cheaters. The most successful functional group across both environments was neither black queens nor cheaters, but those that balanced providing an essential growth-limiting function at a relatively low maintenance cost. Accumulation of loss of function mutants in bulk soil risked resulting in loss of cumulative growth by ToC, while cumulative growth increased in the rhizosphere. In the bulk soil, oligotrophic adaptations assisted species in avoiding extinction. This demonstrated that loss of function by mutation is a successful evolutionary strategy in host-associated and/or resource-rich environments, but poses a risk to communities that must co-operate with each other for mutual co-existence. It was concluded that microbial communities must follow different evolutionary and community assembly strategies in bulk soil versus rhizosphere, with bulk soil communities more dependent on traits that promote co-operative interactions between microbial species.