Repeated, selection-driven genome reduction of accessory genes in experimental populations.

Repeated, selection-driven genome reduction of accessory genes in experimental populations.
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DOI:
10.1371/journal.pgen.1002651
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发表时间:
2012
期刊:
影响因子:
4.5
通讯作者:
Marx CJ
Marx CJ
中科院分区:
生物学2区
文献类型:
--
作者:
Lee MC;Marx CJ

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在许多适应特殊环境的细菌谱系中观察到基因组减少。专性病原体和共生体的基因组极端退化似乎是由遗传漂变主导的。相比之下,对于基因组减少的自由生活的生物体来说,主导力量被认为是对较小的、精简的基因组的直接选择。这些自由生活物种的基因内容的大多数变异是“附属”基因,这些基因通常作为大的染色体岛获得,这些染色体岛适应致病性等特殊性状。然而,目前尚不清楚辅助基因丢失的过程主要是由漂移还是选择驱动的。在这里,我们证明了基因丢失的选择,而不是缩短的基因组本身,导致了辅助基因的大规模、快速减少。在短短 1,500 代的实验进化中,80% 的扭扭甲基杆菌 AM1 群体经历了几乎平行的缺失,从该菌株中存在的巨质粒中去除了多达 10% 的基因组。在突变积累实验中没有这些缺失事件表明选择而不是漂移主导了该过程。重建这些删除证实它们在选择性机制中是有益的,但导致在替代环境中性能下降。这些结果表明,在适应特定环境的早期阶段,选择对于消除不必要的基因至关重要。众所周知,许多自由生活的细菌通常会丢失大部分基因组,但尚不清楚是什么进化力量驱动了这些变化。这是由于小群体的随机损失(被认为是细胞内共生体基因组极端退化的情况)还是由于选择?如果它是有益的,它是否是由复制较短的基因组或基因本身的有利损失直接引起的?我们发现,在实验室进化了 1,500 代的扭扭甲基杆菌 AM1 的大多数复制群体丢失了近 10% 的基因组。通过重建这些缺失,我们证明这些损失确实是有益的,但这种优势并不会随着基因组损失的长度而扩大,在替代环境中甚至是有害的。这些发现表明,基因组收缩的初始阶段可能是由选择驱动的,最终导致更精简、更专业的生物体。
Genome reduction has been observed in many bacterial lineages that have adapted to specialized environments. The extreme genome degradation seen for obligate pathogens and symbionts appears to be dominated by genetic drift. In contrast, for free-living organisms with reduced genomes, the dominant force is proposed to be direct selection for smaller, streamlined genomes. Most variation in gene content for these free-living species is of “accessory” genes, which are commonly gained as large chromosomal islands that are adaptive for specialized traits such as pathogenicity. It is generally unclear, however, whether the process of accessory gene loss is largely driven by drift or selection. Here we demonstrate that selection for gene loss, and not a shortened genome, per se, drove massive, rapid reduction of accessory genes. In just 1,500 generations of experimental evolution, 80% of populations of Methylobacterium extorquens AM1 experienced nearly parallel deletions removing up to 10% of the genome from a megaplasmid present in this strain. The absence of these deletion events in a mutation accumulation experiment suggested that selection, rather than drift, has dominated the process. Reconstructing these deletions confirmed that they were beneficial in their selective regimes, but led to decreased performance in alternative environments. These results indicate that selection can be crucial in eliminating unnecessary genes during the early stages of adaptation to a specialized environment. Many free-living bacteria are known to commonly lose large portions of their genomes, but it is unclear what evolutionary forces drive these changes. Is this due to random loss in small populations, as is thought to be the case for the extreme genome degradation of intracellular symbionts, or due to selection? And if it is beneficial, is it directly caused by replicating a shorter genome or advantageous loss of the genes themselves? We uncovered that most replicate populations of Methylobacterium extorquens AM1 evolved in the laboratory for 1,500 generations lost nearly 10% of their genome. Through reconstructing these deletions, we demonstrated that these losses were indeed beneficial, but the advantage did not scale with length of genome lost, and were even deleterious in alternative environments. These findings suggest that the initial stages of genome shrinkage may be driven by selection, ultimately leading to a more streamlined, specialized organism.
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