Abstract:

Bacterial group I introns are diverse non-coding RNA elements that play significant roles in microbial genome plasticity and ecological adaptation. However, their evolutionary dynamics and ecological roles remain poorly understood. This study conducted a large-scale computational analysis of 40,924 bacterial genomes from the NCBI RefSeq database, revealing 20,554 group I introns across 14 subtypes, with over 99% representing novel sequences. Strikingly, our exploration of marine ecosystems through the TARA Oceans metagenomes uncovered a high prevalence of group I introns in aquatic microbiomes, particularly among cyanobacteria—an evolutionarily ancient lineage critical to marine primary productivity. These marine-derived introns exhibited unique structural diversity and were frequently associated with phage predation networks, as evidenced by a strong correlation between bacterial and viral intron distributions (r = 0.93, p < 1e-08). Furthermore, intron-carrying bacterial genomes in marine environments showed significant co-occurrence with antibiotic resistance genes (ARGs) and virulence factors, suggesting their potential role in enhancing microbial fitness under ecological stress. By integrating data from the Genomes from Earth’s Microbiomes (GEM) catalog, we demonstrated that aquatic niches, especially oceans, serve as hotspots for intron diversity, likely driven by phage-mediated horizontal transfer and host-pathogen coevolution. This study presents the first global atlas of bacterial group I introns, providing essential insights into their evolutionary origins, ecological drivers, and potential roles in microbial genome plasticity. It offers new perspectives for exploiting these elements in genome engineering and antimicrobial strategies. 

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