Director, Institute of Forest Growth and Forest Computer Sciences Technische Universität Dresden, Germany
The identification of mechanisms driving species coexistence and community assembly still belongs to the key challenges addressed for various biotic communities and has been experiencing a rise with agent-based modelling and the consideration of intra-specific variability and multi-level interactions. In microbiomes, many bacterial species have only a very small core genome. Instead, plasmids, which are extrachromosomal genetic elements that replicate autonomously and that can be highly mobile between individual cells, represent a key source of genetic variation. Here we explore the mechanisms that help to preserve the large accessory gene pool that is mediated by plasmids as a fundamental basis for bacterial adaptation. How does intra- and intercellular competition between diverse plasmid types affect the evolution of plasmid communities? Which plasmid identities and traits are maintained under neutral environmental conditions? And how does environmental filtering of specific traits affect community assembly and resilience? To address these questions, an agent-based model of the plasmidome is developed and used to perform a number of simulation experiments. In addition, robustness tests are applied to check if the results are stable to variations in multiple model assumptions.
Our results indicate that community assembly is characterized by deterministic convergence in key plasmid traits and stochastic divergence in plasmid identity. While evolved plasmid communities give rise to cyclic dynamics of bacteria carrying plasmids differing in cost and mobility traits, an emergent system feature that promotes the local coexistence of diverse plasmid types, divergent plasmid identities are established in independent communities due to historical contingency of initial frequency-dependent selection. Niche differentiation through alternative mechanisms of plasmid replication further increases diversity, but the richness of plasmid identities is limited by space, as plasmid resource consumption and emerging spatial structures impose constraints. When environmental filtering is present, an enhanced niche differentiation is required to maintain a high plasmid diversity. If abiotic selection subsequently ceases, communities with higher diversity are more resilient and even promote persistence of traits such as plasmid-mediated antibiotic resistance, whose fitness declines after abiotic selection ended. In summary, this work demonstrates how key plasmid traits mediate eco-evolutionary processes in plasmidomes that promote and preserve the huge genetic diversity required for bacterial communities to adapt to unpredictable changes of environmental conditions. These traits are therefore assumed to be themselves favored by evolutionary selection at the system level.