Evolutionary dynamics of Tn916 in Streptococcus oralis: Fitness cost and persistent metabolic shifts post-acquisition

Abstract

Objectives: The acquisition and transfer of mobile genetic elements (MGEs) are major drivers of antibiotic resistance in bacterial populations. Despite the fitness cost associated with the acquisition of MGEs, the mechanisms underlying their persistence remain poorly understood. This study investigates the evolutionary dynamics of the integrative conjugative element (ICE) Tn916 in a naïve Streptococcus oralis host, focusing on growth rates and metabolic activity. Methods: We tracked the evolutionary trajectory of Tn916 in S. oralis by monitoring changes in growth rates and maximum metabolic activities over 1000 generations. Comparative analyses were conducted between Tn916-free and Tn916-carrying populations to assess fitness cost and evolutionary adaptations. Results: Following Tn916 integration, the S. oralis host exhibited a significant initial fitness cost, characterized by reduced growth rates and maximum metabolic activity. However, within 500 generations, the fitness cost was mitigated, and by 1000 generations, evolved Tn916- transconjugant populations outcompeted their unevolved counterparts. Despite the restoration of growth rates, a persistent reduction in maximum metabolic rate was observed, suggesting resource reallocation favoring growth and ICE maintenance. Conclusion: The acquisition of Tn916 imposes initial fitness cost on S. oralis, but the cost is rapidly mitigated through evolution, leading to competitive advantages in the long term. However, the persistence of lower maximum metabolic rate indicates that Tn916 acquisition affects cellular functions beyond growth, underscoring the need to monitor metabolic activity to fully understand the impact of horizontal gene transfer, MGEs, and ICEs on bacterial populations.