Timing of integration into the chromosome is critical for the fitness of an integrative and conjugative element and its bacterial host.
Timing of integration into the chromosome is critical for the fitness of an integrative and conjugative element and its bacterial host.
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DOI：
10.1371/journal.pgen.1010524
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发表时间：
2023-02
期刊：
影响因子：
4.5
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中科院分区：
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整合和接合元件（ICE）是细菌基因组可塑性的主要贡献者。ICE整合在宿主细菌的染色体中，并在染色体复制和细胞分裂期间被动繁殖。当被激活时，ICE从染色体上切除，并可以通过ICE编码的缀合机制转移到受体细胞中。整合到新宿主的染色体中产生稳定的接合子。虽然整合到新宿主的染色体中对于ICE的稳定获得是至关重要的，但是很少有研究直接研究在稳定的transconjugant的产生期间在受体细胞中发生的分子事件。我们发现，整合ICEBs 1，一个ICE的枯草芽孢杆菌，发生几代后，最初转移到一个新的主机。在新宿主中的过早整合导致细胞死亡，从而降低ICE和transconjugants的适应性。由于过早整合导致的宿主致死性是由在整合的ICEBs 1中启动并延伸到宿主染色体中的滚环复制引起的，从而导致灾难性的基因组不稳定性。我们的研究结果表明，ICE的整合时间与ICE的自主复制的停止有关，并且扰乱这种联系会导致ICE和宿主适应性的降低，这是由于transconjugants的活力丧失。将整合与自主复制的停止联系起来似乎是移动的遗传元件既复制又整合到其宿主染色体中的保守调控方案。水平基因转移对微生物进化有重要贡献，使细菌能够快速获得新的基因和性状。整合和接合元件（Integrative and conjugative elements，ICE）是整合在宿主细菌染色体中的移动的遗传元件，并且可以通过称为接合的接触依赖性机制转移到其他细胞。一些ICE含有赋予其细菌宿主重要性状的基因，包括抗生素抗性、代谢能力和致病性。ICE和其他移动的遗传因子的传播的核心是在传播到新宿主和在宿主内维持之间的平衡，同时最大限度地减少施加在它们的宿主上的适合度负担。我们描述了一种潜在的调控机制，该机制允许已经进入新生宿主的ICE在整合到染色体中之前复制并潜在地传播到其他宿主。整合发生在ICE复制停止后不久或伴随ICE复制停止。这种调节联系的中断导致宿主和ICE的过早整合和适应性缺陷;宿主的致命性和ICE的传播减少。
Integrative and conjugative elements (ICEs) are major contributors to genome plasticity in bacteria. ICEs reside integrated in the chromosome of a host bacterium and are passively propagated during chromosome replication and cell division. When activated, ICEs excise from the chromosome and may be transferred through the ICE-encoded conjugation machinery into a recipient cell. Integration into the chromosome of the new host generates a stable transconjugant. Although integration into the chromosome of a new host is critical for the stable acquisition of ICEs, few studies have directly investigated the molecular events that occur in recipient cells during generation of a stable transconjugant. We found that integration of ICEBs1, an ICE of Bacillus subtilis, occurred several generations after initial transfer to a new host. Premature integration in new hosts led to cell death and hence decreased fitness of the ICE and transconjugants. Host lethality due to premature integration was caused by rolling circle replication that initiated in the integrated ICEBs1 and extended into the host chromosome, resulting in catastrophic genome instability. Our results demonstrate that the timing of integration of an ICE is linked to cessation of autonomous replication of the ICE, and that perturbing this linkage leads to a decrease in ICE and host fitness due to a loss of viability of transconjugants. Linking integration to cessation of autonomous replication appears to be a conserved regulatory scheme for mobile genetic elements that both replicate and integrate into the chromosome of their host. Horizontal gene transfer contributes significantly to microbial evolution, enabling bacteria to rapidly acquire new genes and traits. Integrative and conjugative elements (ICEs) are mobile genetic elements that reside integrated in the chromosome of a host bacterium and can transfer to other cells via a contact-dependent mechanism called conjugation. Some ICEs contain genes that confer important traits to their bacterial hosts, including antibiotic resistances, metabolic capabilities, and pathogenicity. Central to the propagation of ICEs and other mobile genetic elements is the balance between dissemination to new hosts and maintenance within a host, while minimizing the fitness burden imposed on their hosts. We describe an underlying regulatory mechanism that allows for an ICE that has entered into a nascent host to replicate and potentially spread to other hosts before integration into the chromosome. Integration occurs shortly after or concomitant with cessation of ICE replication. Disruption of this regulatory link results in premature integration and fitness defects for both the host and the ICE; lethality for the host and reduced spread of the ICE.
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