Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes.

Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes.
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DOI:
10.1371/journal.pgen.1001284
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发表时间:
2011-01-27
期刊:
影响因子:
4.5
通讯作者:
Rocha EP
Rocha EP
中科院分区:
生物学2区
文献类型:
--
作者:
Treangen TJ;Rocha EP

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基因复制后的新功能或亚功能化深刻影响蛋白质家族的进化,并被认为是真核生物适应性功能新颖性的主要来源。虽然有充足的证据表明原核生物中存在适应性基因复制,但尚不清楚复制是否超过水平基因转移在蛋白质家族扩展中的贡献。我们分析了具有小基因组(螺杆菌、奈瑟菌、链球菌、硫化叶菌)、中等大小基因组(芽孢杆菌、肠杆菌科)和大基因组(假单胞菌、缓生根瘤菌科)密切相关的原核生物菌株或物种,以阐明复制和水平转移的影响。在消除转座元件和噬菌体的影响后,我们发现绝大多数蛋白质家族的扩展都是由于转移,即使在大型基因组中也是如此。转移的基因(异种同源物)在原核谱系中持续时间更长,可能是由于更高/更长的适应性作用。另一方面,重复的基因(旁系同源基因)表达得更多,并且当持续存在时,它们进化得更慢。这表明基因转移和基因复制在塑造生物系统的进化方面具有非常不同的作用:转移允许获得新功能,而复制则导致更高的基因剂量。因此,我们表明旁系同源物共享大多数蛋白质-蛋白质相互作用和遗传调节因子,而异种同源物共享其中很少。原核生物发明了生命的大部分生化多样性。因此,生物系统进化的研究应该明确解释水平基因转移在蛋白质家族多样化中的主导作用。原核生物存在于地球上最多样化和最严峻的生态位中。它们的快速适应在一定程度上是水平获取遗传信息能力的结果。这意味着原核生物利用两条主要途径来扩展其蛋白质家族库:它们可以复制预先存在的基因或通过水平转移获得它。在这项研究中,我们追踪了密切相关的原核物种菌株的家族扩张。我们发现大多数基因扩展是通过转移而不是通过复制实现的。此外,我们发现重复基因往往比转移基因更短暂且进化更慢,突出了在适应和进化方面的不同作用。这些结果表明,旨在理解基于基因复制的生物系统进化的流行理论可能不太适合解释原核系统的进化,其中包括生命的绝大多数生化多样性。
Gene duplication followed by neo- or sub-functionalization deeply impacts the evolution of protein families and is regarded as the main source of adaptive functional novelty in eukaryotes. While there is ample evidence of adaptive gene duplication in prokaryotes, it is not clear whether duplication outweighs the contribution of horizontal gene transfer in the expansion of protein families. We analyzed closely related prokaryote strains or species with small genomes (Helicobacter, Neisseria, Streptococcus, Sulfolobus), average-sized genomes (Bacillus, Enterobacteriaceae), and large genomes (Pseudomonas, Bradyrhizobiaceae) to untangle the effects of duplication and horizontal transfer. After removing the effects of transposable elements and phages, we show that the vast majority of expansions of protein families are due to transfer, even among large genomes. Transferred genes—xenologs—persist longer in prokaryotic lineages possibly due to a higher/longer adaptive role. On the other hand, duplicated genes—paralogs—are expressed more, and, when persistent, they evolve slower. This suggests that gene transfer and gene duplication have very different roles in shaping the evolution of biological systems: transfer allows the acquisition of new functions and duplication leads to higher gene dosage. Accordingly, we show that paralogs share most protein–protein interactions and genetic regulators, whereas xenologs share very few of them. Prokaryotes invented most of life's biochemical diversity. Therefore, the study of the evolution of biology systems should explicitly account for the predominant role of horizontal gene transfer in the diversification of protein families. Prokaryotes can be found in the most diverse and severe ecological niches of the planet. Their rapid adaptation is, in part, the result of the ability to acquire genetic information horizontally. This means that prokaryotes utilize two major paths to expand their repertoire of protein families: they can duplicate a pre-existing gene or acquire it by horizontal transfer. In this study, we track family expansions among closely related strains of prokaryotic species. We find that the majority of gene expansions arrive via transfer not via duplication. Additionally, we find that duplicate genes tend be more transient and evolve slower than transferred ones, highlighting different roles with respect to adaptation and evolution. These results suggest that prevailing theories aimed at understanding the evolution of biological systems grounded on gene duplication might be poorly fit to explain the evolution of prokaryotic systems, which include the vast majority of life's biochemical diversity.
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