Predicting the minimal translation apparatus: lessons from the reductive evolution of mollicutes.
Predicting the minimal translation apparatus: lessons from the reductive evolution of mollicutes.
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DOI：
10.1371/journal.pgen.1004363
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发表时间：
2014-05
期刊：
影响因子：
4.5
通讯作者：
Blanchard A
中科院分区：
文献类型：
--
作者：
Grosjean H;Breton M;Sirand-Pugnet P;Tardy F;Thiaucourt F;Citti C;Barré A;Yoshizawa S;Fourmy D;de Crécy-Lagard V;Blanchard A
莫利库斯是一类寄生细菌，主要是通过大规模的基因组减少而从普通的菲米库斯祖先进化而来的。由于基因组大小不到1 MBP，大多数Mollicus物种保留了复制和自主生长的能力。这项工作的主要目标是确定在这些细菌中能够维持核糖体生物发生和遗传密码翻译的最小蛋白质集。使用实验验证的模式菌大肠杆菌和枯草芽孢杆菌的基因作为输入，预测了39个不同的Mollicus物种的核心翻译机制蛋白编码基因，其中33个是可培养的。这组260个输入基因编码了核糖体生物发生、tRNA成熟和氨基酰化过程中涉及的蛋白质，以及mRNA翻译和RNA衰退所需的蛋白质辅助因子。在所有被分析的物种中都发现了104种这些蛋白质的核心集合。在核糖体组装和RNA降解中，涉及核糖体蛋白和翻译辅助因子的翻译后修饰、t+rRNA的转录后修饰和RNA降解的编码蛋白的基因是最常丢失的。不出所料，编码氨基酰-tRNA合成酶、核糖体蛋白以及起始、延伸和终止因子的基因是最持久的(即在大多数基因组中保守)。在tRNA的反密码子环、16S rRNA的螺旋44和23S rRNA的螺旋69和80中引入核苷酸修饰的酶在所有物种中都是必不可少的，这些都是解码和促进肽转移所必需的。对Mollicuts基因组进化的重建显示，除了许多基因丢失外，偶尔也会出现水平基因转移的收益。这一分析不仅表明，在接下来的几轮还原进化中，出现了略有不同的保留功能的、尽管是最小的蛋白质合成机制的解决方案，而且在指导合成生物学方法重建最小细胞方面也具有广泛的意义。在所有细胞中，蛋白质都是通过涉及许多蛋白质和RNA的复杂机制，从信使核糖核酸编码的信息中合成的。在这个称为翻译的过程中，核糖体起着核心作用。从最简单的细菌到哺乳动物细胞，参与核糖体生物发生及其功能的元件在所有生物体中都是极其保守的。在已知的260种参与翻译的蛋白质中，大多数都是在大肠杆菌和枯草芽孢杆菌这两种生物学中常见的细胞模型中识别和研究的。然而，比较基因组学已经表明，翻译蛋白质集可以小得多。这一点适用于属于双目的细菌，它们的特征是基因组减少，因此被认为是最小细胞的模型。通过同源推理和专家分析，我们鉴定了其中39种生物的翻译装置蛋白。尽管在不同的物种之间发现了惊人的差异，但一些莫利库斯物种所需的蛋白质只有大肠杆菌或枯草杆菌的一半。这一分析使我们能够确定在Mollicuts中翻译所需的一组蛋白质，并定义在模仿最小细菌细胞的细胞底盘中所需的翻译装置。
Mollicutes is a class of parasitic bacteria that have evolved from a common Firmicutes ancestor mostly by massive genome reduction. With genomes under 1 Mbp in size, most Mollicutes species retain the capacity to replicate and grow autonomously. The major goal of this work was to identify the minimal set of proteins that can sustain ribosome biogenesis and translation of the genetic code in these bacteria. Using the experimentally validated genes from the model bacteria Escherichia coli and Bacillus subtilis as input, genes encoding proteins of the core translation machinery were predicted in 39 distinct Mollicutes species, 33 of which are culturable. The set of 260 input genes encodes proteins involved in ribosome biogenesis, tRNA maturation and aminoacylation, as well as proteins cofactors required for mRNA translation and RNA decay. A core set of 104 of these proteins is found in all species analyzed. Genes encoding proteins involved in post-translational modifications of ribosomal proteins and translation cofactors, post-transcriptional modifications of t+rRNA, in ribosome assembly and RNA degradation are the most frequently lost. As expected, genes coding for aminoacyl-tRNA synthetases, ribosomal proteins and initiation, elongation and termination factors are the most persistent (i.e. conserved in a majority of genomes). Enzymes introducing nucleotides modifications in the anticodon loop of tRNA, in helix 44 of 16S rRNA and in helices 69 and 80 of 23S rRNA, all essential for decoding and facilitating peptidyl transfer, are maintained in all species. Reconstruction of genome evolution in Mollicutes revealed that, beside many gene losses, occasional gains by horizontal gene transfer also occurred. This analysis not only showed that slightly different solutions for preserving a functional, albeit minimal, protein synthetizing machinery have emerged in these successive rounds of reductive evolution but also has broad implications in guiding the reconstruction of a minimal cell by synthetic biology approaches. In all cells, proteins are synthesized from the message encoded by mRNA using complex machineries involving many proteins and RNAs. In this process, named translation, the ribosome plays a central role. The elements involved in both ribosome biogenesis and its function are extremely conserved in all organisms from the simplest bacteria to mammalian cells. Most of the 260 known proteins involved in translation have been identified and studied in the bacteria Escherichia coli and Bacillus subtilis, two common cellular models in biology. However, comparative genomics has shown that the translation protein set can be much smaller. This is true for bacteria belonging to the class Mollicutes that are characterized by reduced genomes and hence considered as models for minimal cells. Using homology inference approach and expert analyses, we identified the translation apparatus proteins for 39 of these organisms. Although striking variations were found from one group of species to another, some Mollicutes species require half as many proteins as E. coli or B. subtilis. This analysis allowed us to determine a set of proteins necessary for translation in Mollicutes and define the translation apparatus that would be required in a cellular chassis mimicking a minimal bacterial cell.
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