Bacterial origin of a key innovation in the evolution of the vertebrate eye.

Bacterial origin of a key innovation in the evolution of the vertebrate eye.
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DOI:
10.1073/pnas.2214815120
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发表时间:
2023-04-18
影响因子:
11.1
通讯作者:
Daugherty, Matthew D.
Daugherty, Matthew D.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Kalluraya, Chinmay A.;Weitzel, Alexander J.;Tsu, Brian V.;Daugherty, Matthew D.

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自查尔斯·达尔文时代以来,解释眼睛的逐步进化一直是一个挑战。在这里,我们描述了细菌通过域间水平基因转移(iHGT)对脊椎动物眼睛进化的重要贡献,该细菌基因产生了脊椎动物特异性光感受器间视黄醇结合蛋白(IRBP)。我们证明,IRBP 是一种高度保守且必需的类视黄醇穿梭蛋白,源自细菌基因,该基因是在脊椎动物型眼睛 > 500 Mya 的发育过程中获得、复制和新功能化的。重要的是,我们的研究结果为像脊椎动物眼睛这样的复杂结构的进化提供了一条途径:不仅通过修补现有的遗传物质,还通过获取和功能性整合外来基因。查尔斯·达尔文将脊椎动物的眼睛描述为对逐步进化过程的自然选择理论的最大潜在挑战之一。虽然导致脊椎动物眼睛的许多进化转变已经得到解释,但某些方面似乎是脊椎动物特有的,没有明显的后生动物前身。脊椎动物和无脊椎动物视觉之间的一个关键区别取决于光感受器间类视黄醇结合蛋白(IRBP,也称为视黄醇结合蛋白,RBP3),它通过促进类视黄醇在细胞类型之间的穿梭,实现脊椎动物视觉周期中细胞的物理分离和专门化。虽然 IRBP 的功能已得到描述,但其进化起源仍然难以捉摸。在这里,我们证明 IRBP 是通过域间水平基因转移 (iHGT) 从细菌中获取新的遗传物质而产​​生的。我们证明编码细菌肽酶的基因是在对现存脊椎动物> 500 Mya进行辐射之前获得的,并经历了随后的结构域复制和新功能化以产生脊椎动物IRBP。我们对生命树中超过 900 个高质量基因组进行的系统发育分析提供了区分基因组组装中的污染与 IRBP 水平获取的真实实例的分辨率,并使我们发现相同细菌肽酶基因家族向不同真核谱系的额外独立转移。重要的是,这项工作阐明了导致脊椎动物视觉周期的关键转变的进化基础,并强调了细菌基因的获取对脊椎动物进化的显着影响。
Since the time of Charles Darwin, explaining the stepwise evolution of the eye has been a challenge. Here, we describe the essential contribution of bacteria to the evolution of the vertebrate eye, via interdomain horizontal gene transfer (iHGT), of a bacterial gene that gave rise to the vertebrate-specific interphotoreceptor retinoid-binding protein (IRBP). We demonstrate that IRBP, a highly conserved and essential retinoid shuttling protein, arose from a bacterial gene that was acquired, duplicated, and neofunctionalized coincident with the development of the vertebrate-type eye >500 Mya. Importantly, our findings provide a path by which complex structures like the vertebrate eye can evolve: not just by tinkering with existing genetic material, but also by acquiring and functionally integrating foreign genes. The vertebrate eye was described by Charles Darwin as one of the greatest potential challenges to a theory of natural selection by stepwise evolutionary processes. While numerous evolutionary transitions that led to the vertebrate eye have been explained, some aspects appear to be vertebrate specific with no obvious metazoan precursor. One critical difference between vertebrate and invertebrate vision hinges on interphotoreceptor retinoid-binding protein (IRBP, also known as retinol-binding protein, RBP3), which enables the physical separation and specialization of cells in the vertebrate visual cycle by promoting retinoid shuttling between cell types. While IRBP has been functionally described, its evolutionary origin has remained elusive. Here, we show that IRBP arose via acquisition of novel genetic material from bacteria by interdomain horizontal gene transfer (iHGT). We demonstrate that a gene encoding a bacterial peptidase was acquired prior to the radiation of extant vertebrates >500 Mya and underwent subsequent domain duplication and neofunctionalization to give rise to vertebrate IRBP. Our phylogenomic analyses on >900 high-quality genomes across the tree of life provided the resolution to distinguish contamination in genome assemblies from true instances of horizontal acquisition of IRBP and led us to discover additional independent transfers of the same bacterial peptidase gene family into distinct eukaryotic lineages. Importantly, this work illustrates the evolutionary basis of a key transition that led to the vertebrate visual cycle and highlights the striking impact that acquisition of bacterial genes has had on vertebrate evolution.
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发表时间: 2017-05-08
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影响因子: 12.3
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影响因子: 56.9
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影响因子: 2.1
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