Chromosome structuring limits genome plasticity in Escherichia coli.

Chromosome structuring limits genome plasticity in Escherichia coli.
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DOI:
10.1371/journal.pgen.0030226
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发表时间:
2007-12
期刊:
影响因子:
4.5
通讯作者:
Boccard F
Boccard F
中科院分区:
生物学2区
文献类型:
--
作者:
Esnault E;Valens M;Espéli O;Boccard F

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尽管有很长的分化期,但相关细菌属的染色体组织保持得很好。我们已经评估了限制细菌基因组可塑性在大肠杆菌中的力量,通过测量改变不同的参数,包括DNA复制,组成偏斜的replichores,协调基因表达与DNA复制,复制相关的基因剂量,和染色体组织成macrodomains的各自的效果。染色体发生大倒位重排。复制区的组成偏差、基因表达与DNA复制的协调或复制相关基因剂量的变化对细胞生理学仅产生中度影响,因为逆转复制区内数百个基因方向的大规模重排只是轻微有害。相比之下,改变两个复制臂之间的平衡具有更剧烈的效果,并且当其中一个染色体臂小于另一个染色体臂的一半时,细胞活力需要复制叉的重组拯救。宏结构域组织似乎也是限制染色体可塑性的主要因素,两种类型的倒置构型严重影响细胞周期。首先,Ter宏结构域的破坏与复制叉合并远离正常的replichore连接引起染色体分离缺陷。第二个主要的有问题的配置导致从Ori和右宏域之间的反转,扰动类核分布和胞质分裂的早期步骤。细菌细胞周期的控制和细菌染色体构型的进化的后果进行了讨论。基因组学分析表明,细菌基因组是动态实体,通过各种过程进化,包括染色体内遗传重排,基因复制和基因丢失或通过基因转移获得。尽管如此,从相关属细菌染色体的比较揭示了遗传组织的保守性。大多数细菌基因组是环状分子,DNA复制从一个起点到复制叉相遇的相对区域进行双向复制。复制过程在细菌染色体上留下印记,因为在限定的基因座处的起始和终止由于在前导链和滞后链合成期间发生的突变差异而导致链偏差。我们分析了可能限制基因组可塑性的不同参数的强度。我们发现,优先定位的主导链上的必需基因,参与转录和翻译的基因的接近的主导链上的复制起点,和存在偏见的图案沿着复制操作只作为长期的积极选择的决定因素。相比之下,选择的作用是维持相似长度的复制臂。最后,我们证明了染色体的空间结构阻碍了基因组的可塑性。遗传学证据支持细胞周期中存在由染色体空间组织控制的两个步骤。
Chromosome organizations of related bacterial genera are well conserved despite a very long divergence period. We have assessed the forces limiting bacterial genome plasticity in Escherichia coli by measuring the respective effect of altering different parameters, including DNA replication, compositional skew of replichores, coordination of gene expression with DNA replication, replication-associated gene dosage, and chromosome organization into macrodomains. Chromosomes were rearranged by large inversions. Changes in the compositional skew of replichores, in the coordination of gene expression with DNA replication or in the replication-associated gene dosage have only a moderate effect on cell physiology because large rearrangements inverting the orientation of several hundred genes inside a replichore are only slightly detrimental. By contrast, changing the balance between the two replication arms has a more drastic effect, and the recombinational rescue of replication forks is required for cell viability when one of the chromosome arms is less than half than the other one. Macrodomain organization also appears to be a major factor restricting chromosome plasticity, and two types of inverted configurations severely affect the cell cycle. First, the disruption of the Ter macrodomain with replication forks merging far from the normal replichore junction provoked chromosome segregation defects. The second major problematic configurations resulted from inversions between Ori and Right macrodomains, which perturb nucleoid distribution and early steps of cytokinesis. Consequences for the control of the bacterial cell cycle and for the evolution of bacterial chromosome configuration are discussed. Genomic analyses have revealed that bacterial genomes are dynamic entities that evolve through various processes including intrachromosome genetic rearrangements, gene duplication, and gene loss or acquisition by gene transfer. Nevertheless, comparison of bacterial chromosomes from related genera revealed a conservation of genetic organization. Most bacterial genomes are circular molecules, and DNA replication proceeds bidirectionally from a single origin to an opposite region where replication forks meet. The replication process imprints the bacterial chromosome because initiation and termination at defined loci result in strand biases due to the mutational differences occurring during leading and lagging strands synthesis. We analyze the strength of different parameters that may limit genome plasticity. We show that the preferential positioning of essential genes on the leading strand, the proximity of genes involved in transcription and translation to the origin of replication on the leading strand, and the presence of biased motifs along the replichores operate only as long-term positive selection determinants. By contrast, selection operates to maintain replication arms of similar lengths. Finally, we demonstrate that spatial structuring of the chromosome impedes strongly genome plasticity. Genetic evidence supports the presence of two steps in the cell cycle controlled by the spatial organization of the chromosome.
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