Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, Russia.
Pertsov White Sea Biological Station, Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia.
Genome Biol Evol. 2023 Dec 1;15(12). doi: 10.1093/gbe/evad219.
Most characterized metazoan mitochondrial genomes are compact and encode a small set of proteins that are essential for oxidative phosphorylation, as well as rRNA and tRNA for their expression. However, in rare cases, invertebrate taxa have additional open reading frames (ORFs) in their mtDNA sequences. Here, we sequenced and analyzed the mitochondrial genome of a polychaete worm, Polydora cf. ciliata, part of whose life cycle takes place in low-oxygen conditions. In the mitogenome, we found three "ORFan" regions (544, 1,060, and 427 bp) that have no resemblance to any standard metazoan mtDNA gene but lack stop codons in one of the reading frames. Similar regions are found in the mitochondrial genomes of three other Polydora species and Bocardiella hamata. All five species share the same gene order in their mitogenomes, which differ from that of other known Spionidae mitogenomes. By analyzing the ORFan sequences, we found that they are under purifying selection pressure and contain conservative regions. The codon adaptation indices (CAIs) of the ORFan genes were in the same range of values as the CAI of conventional protein-coding genes in corresponding mitochondrial genomes. The analysis of the P. cf. ciliata mitochondrial transcriptome showed that ORFan-544, ORFan-427, and a portion of the ORFan-1060 are transcribed. Together, this suggests that ORFan-544 and ORFan-427 encode functional proteins. It is likely that the ORFans originated when the Polydora/Bocardiella species complex separated from the rest of the Spionidae, and this event coincided with massive gene rearrangements in their mitochondrial genomes and tRNA-Met duplication.
大多数特征明显的后生动物线粒体基因组都很紧凑，只编码一小部分蛋白质，这些蛋白质对于氧化磷酸化以及 rRNA 和 tRNA 的表达是必不可少的。然而，在极少数情况下，无脊椎动物类群的 mtDNA 序列中存在额外的开放阅读框 (ORF)。在这里，我们对多毛类环节蠕虫 Polydora cf. ciliata 的线粒体基因组进行了测序和分析，其生命周期的一部分发生在低氧条件下。在这个线粒体基因组中，我们发现了三个“ORFan”区域（544、1060 和 427bp），它们与任何标准的后生动物 mtDNA 基因都没有相似之处，但其中一个阅读框缺少终止密码子。在其他三种 Polydora 物种和 Bocardiella hamata 的线粒体基因组中也发现了类似的区域。这五个物种在它们的线粒体基因组中具有相同的基因排列，与其他已知的 Spionidae 线粒体基因组不同。通过分析 ORFan 序列，我们发现它们受到纯化选择压力的影响，并包含保守区域。ORFan 基因的密码子适应指数 (CAI)与相应线粒体基因组中常规蛋白质编码基因的 CAI 值相同。对 P. cf. ciliata 线粒体转录组的分析表明，ORFan-544、ORFan-427 和 ORFan-1060 的一部分被转录。综上所述，这表明 ORFan-544 和 ORFan-427 编码功能性蛋白质。很可能 ORFan 是在 Polydora/Bocardiella 种复合体与 Spionidae 的其他物种分离时起源的，而这一事件与它们的线粒体基因组和 tRNA-Met 重复的大规模基因重排同时发生。
