How a Genetically Stable Extremophile Evolves: Modes of Genome Diversification in the Archaeon Sulfolobus acidocaldarius
How a Genetically Stable Extremophile Evolves: Modes of Genome Diversification in the Archaeon Sulfolobus acidocaldarius
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DOI：
10.1128/jb.00177-17
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发表时间：
2017-09-01
影响因子：
3.2
通讯作者：
Grogan, Dennis W.
中科院分区：
文献类型：
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作者：
Mao, Dominic;Grogan, Dennis W.
为了从分子水平上分析硫化叶菌基因组是如何分化的，分别在酸热硫化叶菌的实验室构建体和野生型分离株中鉴定了损伤诱导的突变和天然多态性（PM）。在从一个当地种群中提取的野生型分离株中，成对核苷酸分歧平均为4 × 10（-6），这是所报道的岛硫化叶菌相应分歧的0.15%左右。野生型S.嗜酸热菌基因组是均聚物（单核苷酸）片段和较长的串联重复序列，与实验室条件下发生的自发突变一致。然而，天然分离株也显示了大的插入/缺失和倒位，这在任何实验室操作的菌株中都没有发生。几个大的插入/缺失可以归因于移动的遗传元件（MGE）的整合或切除，每个MGE代表一个独特的系统的位点特异性重组。与一个MGE（一种与硫化叶菌转塔二十面体病毒相关的前病毒）相关的重组模式也见于某些染色体倒位。化学诱导的突变、非MGE插入/缺失和小PM在基因组上表现出不同的分布，表明硫化叶菌基因组的大规模模式化在趋异过程的早期就开始了。与诱导突变不同，自然碱基对取代发生在簇中，并且一个簇表现出分散的不完美重复之间的非互惠重组（基因转换）的预期特性。综上所述，研究结果表明，简单的复制错误、由串联重复序列促进的滑动链事件、同源重组和由MGE促进的重排是这种极端嗜酸性古菌在地热环境中遗传变异的主要来源。重要性极端嗜热古菌的最佳生长温度加速了DNA的分解，这有望使DNA修复对其遗传稳定性特别重要，但这些古细菌缺乏某些广泛保守的DNA修复蛋白。在这项研究中，极端嗜热嗜酸硫化叶菌的基因组被发现非常稳定，在许多（尽管不是全部）实验室操作和自然种群中积累了很少的突变。此外，所有被推断为使这些基因组多样化的遗传过程也在嗜温细菌和真核生物中运作。这表明，一套共同的机制产生了所有微生物中的大部分遗传变异，尽管在生理学，DNA修复系统和基因组结构方面存在根本差异，这三个领域的生活。
In order to analyze in molecular terms how Sulfolobus genomes diverge, damage-induced mutations and natural polymorphisms (PMs) were identified in laboratory constructs and wild-type isolates, respectively, of Sulfolobus acidocaldarius. Among wild-type isolates drawn from one local population, pairwise nucleotide divergence averaged 4 x 10(-6), which is about 0.15% of the corresponding divergence reported for Sulfolobus islandicus. The most variable features of wild-type S. acidocaldarius genomes were homopolymer (mononucleotide) tracts and longer tandem repeats, consistent with the spontaneous mutations that occur under laboratory conditions. Natural isolates, however, also revealed large insertions/deletions and inversions, which did not occur in any of the laboratory-manipulated strains. Several of the large insertions/deletions could be attributed to the integration or excision of mobile genetic elements (MGEs), and each MGE represented a distinct system of site-specific recombination. The mode of recombination associated with one MGE, a provirus related to Sulfolobus turreted icosahedral virus, was also seen in certain chromosomal inversions. Artificially induced mutations, non-MGE insertions/deletions, and small PMs exhibited different distributions over the genome, suggesting that large-scale patterning of Sulfolobus genomes begins early in the divergence process. Unlike induced mutations, natural base pair substitutions occurred in clusters, and one cluster exhibited properties expected of nonreciprocal recombination (gene conversion) between dispersed imperfect repeats. Taken together, the results identify simple replication errors, slipped-strand events promoted by tandem repeats, homologous recombination, and rearrangements promoted by MGEs as the primary sources of genetic variation for this extremely acidophilic archaeon in its geothermal environment.IMPORTANCE The optimal growth temperatures of hyperthermophilic archaea accelerate DNA decomposition, which is expected to make DNA repair especially important for their genetic stability, yet these archaea lack certain broadly conserved types of DNA repair proteins. In this study, the genome of the extreme thermoacidophile Sulfolobus acidocaldarius was found to be remarkably stable, accumulating few mutations in many (though not all) laboratory manipulations and in natural populations. Furthermore, all the genetic processes that were inferred to diversify these genomes also operate in mesophilic bacteria and eukaryotes. This suggests that a common set of mechanisms produces most of the genetic variation in all microorganisms, despite the fundamental differences in physiology, DNA repair systems, and genome structure represented in the three domains of life.