Department of Animal Biology, University of Illinois at Urbana-Champaign, IL, USA.
Mol Biol Evol. 2010 Jun;27(6):1391-403. doi: 10.1093/molbev/msq026. Epub 2010 Jan 27.
Evolution of Antarctic notothenioids in the frigid and oxygen-rich Southern Ocean had led to remarkable genomic changes, most notably the gain of novel antifreeze glycoproteins and the loss of oxygen-binding hemoproteins in the icefish family. Recently, the mitochondrial (mt) NADH dehydrogenase subunit 6 (ND6) gene and the adjacent transfer RNA(Glu) (tRNA(Glu)) were also reportedly lost. ND6 protein is crucial for the assembly and function of Complex I of the mt electron transport chain that produces adenosine triphosphate (ATP) essential for life; thus, ND6 absence would be irreconcilable with Antarctic notothenioids being thriving species. Here we report our discovery that the ND6 gene and tRNA(Glu) were not lost but had been translocated to the control region (CR) from their canonical location between ND5 and cytochrome b genes. We characterized the CR and adjacent sequences of 22 notothenioid species representing all eight families of Notothenioidei to elucidate the mechanism and evolutionary history of this mtDNA rearrangement. Species of the three basal non-Antarctic families have the canonical vertebrate mt gene order, whereas species of all five Antarctic families have a rearranged CR bearing the embedded ND6 (ND6(CR)) and tRNA(Glu), with additional copies of tRNA(Thr), tRNA(Pro), and noncoding region in various lineages. We hypothesized that an initial duplication of the canonical mt region from ND6 through CR occurred in the common ancestor to the Antarctic clade, and we deduced the succession of loss or modification of the duplicated region leading to the extant patterns of mt DNA reorganization that is consistent with notothenioid evolutionary history. We verified that the ND6(CR) gene in Antarctic notothenioids is transcribed and therefore functional. However, ND6(CR)-encoded protein sequences differ substantially from basal non-Antarctic notothenioid ND6, and we detected lineage-specific positive selection on the branch leading to the Antarctic clade of ND6(CR) under the branch-site model. Collectively, the novel mt ND6(CR) genotype of the Antarctic radiation represents another major molecular change in Antarctic notothenioid evolution and may reflect an adaptive change conducive to the functioning of the protein (Complex I) machinery of mt respiration in the polar environment, driven by the advent of freezing, oxygen-rich conditions in the Southern Ocean.
南极无鳍鱼在寒冷且富含氧气的南大洋中的进化导致了显著的基因组变化，最显著的是在冰鱼科中获得了新型抗冻糖蛋白和失去了氧结合血红素蛋白。最近，线粒体（mt）NADH 脱氢酶亚单位 6（ND6）基因和相邻的转移 RNA（Glu）（tRNA（Glu））也被报道丢失。ND6 蛋白对于 mt 电子传递链复合物 I 的组装和功能至关重要，该复合物产生生命所必需的三磷酸腺苷（ATP）；因此，ND6 的缺失与南极无鳍鱼作为繁荣物种是不可调和的。在这里，我们报告了我们的发现，即 ND6 基因和 tRNA（Glu）并没有丢失，而是已经从 ND5 和细胞色素 b 基因之间的典型位置转移到了控制区（CR）。我们对代表 Notothenioidei 所有 8 个科的 22 种无鳍鱼的 CR 和相邻序列进行了特征描述，以阐明这种 mtDNA 重排的机制和进化历史。三个非南极基础科的物种具有典型的脊椎动物 mt 基因顺序，而所有五个南极科的物种都具有一个重排的 CR，其中包含嵌入的 ND6（ND6（CR））和 tRNA（Glu），以及在不同谱系中的额外的 tRNA（Thr）、tRNA（Pro）和非编码区。我们假设，在南极支系的共同祖先中，从 ND6 到 CR 的典型 mt 区域的初始重复发生，并且我们推断出重复区域的丢失或修饰的连续过程导致了与现存的 mtDNA 重排模式一致的 Notothenioidei 进化历史。我们验证了南极无鳍鱼中的 ND6（CR）基因是可转录的，因此是有功能的。然而，南极无鳍鱼 ND6（CR）编码的蛋白序列与基础非南极无鳍鱼 ND6 有很大的不同，并且我们在分支位点模型下检测到在导致南极支系的分支上 ND6（CR）的正选择。总的来说，南极辐射中新的 mtND6（CR）基因型代表了南极无鳍鱼进化中的另一个主要分子变化，并且可能反映了适应极地环境的 mt 呼吸蛋白（复合物 I）机制的功能变化，这是由南大洋中冻结和富含氧气条件的出现所驱动的。
