Lineage-specific loss of the type VI secretion system in <i>Acinetobacter baumannii</i> ST19 is associated with reduced accessory genome content

The type VI secretion system (T6SS) is a widespread bacterial nanomachine involved in interbacterial competition and environmental adaptation. Its distribution and evolutionary significance in Acinetobacter baumannii is not fully understood. Here, we investigated the ST19 lineage, revealing a near-complete absence of the T6SS across 159 genomes from diverse geographic and clinical origins. Comparative genomic analysis showed that the T6SS locus in ST19 is frequently disrupted, with some isolates harboring insertions of mobile genetic elements, while in others, the region is fragmented or unresolved. To assess whether T6SS loss is associated with broader genomic changes, we analyzed 8,218 publicly available A. baumannii genomes. Interestingly, T6SS-negative genomes did not exhibit increased acquisition of accessory genetic material. Instead, they carried fewer antimicrobial resistance genes (8.06 vs 10.56 per genome), fewer virulence genes (101.8 vs 132.5 per genome), and comparable plasmid replicon content relative to T6SS-positive genomes. However, T6SS-negative genomes exhibited a higher number of insertion sequences (IS) per genome compared to T6SS-positive genomes (mean similar to 12.3 vs similar to 9.0 IS elements per genome, respectively). Ancestral state reconstruction of the frmRAB and the putative chlorite dismutase genes within ST19 revealed identical distribution patterns and strong phylogenetic conservation, with 7 inferred state transitions indicating limited evidence for independent gain or loss events. Our results suggest that T6SS loss represents a lineage-specific evolutionary trajectory characterized by loss of the T6SS locus and reduced accessory genome, suggesting an alternative ecological strategy.