Liu Yang, Botelho João, Iranzo Jaime
Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), 28223, Madrid, Spain.
Centro de Astrobiología (CAB), CSIC-INTA, 28850, Madrid, Spain;
Genome Res. 2025 Feb 14;35(2):268-278. doi: 10.1101/gr.279300.124.
Prokaryotes have evolved a wide repertoire of defense systems to prevent invasion by mobile genetic elements (MGEs). However, because MGEs are vehicles for the exchange of beneficial accessory genes, defense systems could consequently impede rapid adaptation in microbial populations. Here, we study how defense systems impact horizontal gene transfer (HGT) in the short term and long term. By combining comparative genomics and phylogeny-aware statistical methods, we quantify the association between the presence of seven widespread defense systems and the abundance of MGEs in the genomes of 196 bacterial and one archaeal species. We also calculate the differences in the rates of gene gain and loss between lineages that possess and lack each defense system. Our results show that the impact of defense systems on HGT is highly taxon and system dependent and, in most cases, not statistically significant. Timescale analysis reveals that defense systems must persist in a lineage for a relatively long time to exert an appreciable negative impact on HGT. In contrast, for shorter evolutionary timescales, frequent coacquisition of MGEs and defense systems results in a net positive association of the latter with HGT. Given the high turnover rates experienced by defense systems, we propose that the inhibitory effect of most defense systems on HGT is masked by their strong linkage with MGEs. These findings help explain the contradictory conclusions of previous research by pointing at mobility and within-host retention times as key factors that determine the impact of defense systems on genome plasticity.
原核生物已经进化出了广泛的防御系统，以防止移动遗传元件（MGEs）的入侵。然而，由于MGEs是有益辅助基因交换的载体，防御系统可能因此阻碍微生物种群的快速适应。在这里，我们研究防御系统如何在短期和长期内影响水平基因转移（HGT）。通过结合比较基因组学和系统发育感知统计方法，我们量化了196种细菌和1种古菌基因组中7种广泛存在的防御系统的存在与MGEs丰度之间的关联。我们还计算了拥有和缺乏每种防御系统的谱系之间基因获得和丢失速率的差异。我们的结果表明，防御系统对HGT的影响高度依赖于分类群和系统，并且在大多数情况下，没有统计学意义。时间尺度分析表明，防御系统必须在一个谱系中持续存在相对较长的时间，才能对HGT产生明显的负面影响。相比之下，在较短的进化时间尺度上，MGEs和防御系统的频繁共同获得导致后者与HGT呈净正相关。鉴于防御系统的高周转率，我们提出大多数防御系统对HGT的抑制作用被它们与MGEs的强连锁所掩盖。这些发现通过指出移动性和宿主内保留时间是决定防御系统对基因组可塑性影响的关键因素，有助于解释先前研究的矛盾结论。
