Adaptative and ancient co-evolution of integrons withXanthomonasgenomes
Abstract
Integrons are genetic elements that facilitate gene acquisition. They have been extensively studied in clinical bacteria, but their evolutionary role in phytopathogens remains underexplored. Here, we analysed complete genomes ofXanthomonasspecies to investigate the origin, distribution, and functional dynamics of integrons in this genus. We found that 93% of genomes harboured integrons. The integron-integrase geneintIwas predominantly located downstream ofilvD, indicating an ancestral acquisition of integrons, predating diversification within the genus. Phylogenetic analyses support vertical inheritance ofintI, with the exception of rare horizontal gene transfer events, notably inX. arboricola. Despite their widespread presence, full-lengthintIgenes and active integron platforms are only retained in some species, especiallyX. campestris, which shows high integron gene cassette variability and functional integron activity. In contrast, species such asX. cissicolaandX. phaseoliexhibit widespreadinIinactivation, likely occurring early in their divergence, leading to more stable cassette arrays and conserved integron-associated phenotypes. The number and diversity of genes within cassette arrays varied significantly by species and, to a lesser extent, by the ecological context of plant host cultivation. While most cassettes encoded proteins without a known function, those with annotated roles were associated with stress response mechanism, competitive exclusion, and plant-associated functions. Together, our findings demonstrate that integrons inXanthomonaslikely originated from a single ancient acquisition event, preceding genus-wide speciation, and have co-evolved withXanthomonaspathovars as they adapted to distinct plant hosts.
IMPACT STATEMENT
This study provides the first comprehensive genus-wide analysis of integron evolution and dynamics inXanthomonas, a globally distributed and versatile plant pathogen. Integrons are genetic platforms that allow horizontal transfer of genes. They are well characterised in human pathogens where they mediate transfer of antibiotic resistance genes, but little is known about their role in plant associated bacteria. We showed that inXanthomonasthe integron platform was ancestrally acquired, yet integrons have undergone repeated lineage-specific inactivation events. Despite widespread erosion of integron activity, some species such asX. campestrismaintain robust and functionally diverse integrons that continue to shape genome plasticity. Notably, high cassette diversity, combined with the presence of rare and often uncharacterized genes within these arrays (some potentially involved in environmental sensing or host interaction) suggest that integrons may serve as reservoirs of adaptive potential. Our findings reshape current views of integron function beyond antibiotic resistance and highlight their long-term role in microbial evolution, niche adaptation, and genome innovation in plant-associated bacteria.
DATA SUMMARY
The authors confirm all supporting data, code and protocols have been provided within the article or through supplementary data files.
Related articles
Related articles are currently not available for this article.