Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, China.
Shandong University, Qingdao, China.
BMC Genomics. 2022 Dec 7;23(1):809. doi: 10.1186/s12864-022-09040-3.
Arcidae, comprising about 260 species of ark shells, is an ecologically and economically important lineage of bivalve mollusks. Interestingly, mitochondrial genomes of several Arcidae species are 2-3 times larger than those of most bilaterians, and are among the largest bilaterian mitochondrial genomes reported to date. The large mitochondrial genome size is mainly due to expansion of unassigned regions (regions that are functionally unassigned). Previous work on unassigned regions of Arcidae mtDNA genomes has focused on nucleotide-level analyses to observe sequence characteristics, however the origin of expansion remains unclear.
We assembled six new mitogenomes and sequenced six transcriptomes of Scapharca broughtonii to identify conserved functional ORFs that are transcribed in unassigned regions. Sixteen lineage-specific ORFs with different copy numbers were identified from seven Arcidae species, and 11 of 16 ORFs were expressed and likely biologically active. Unassigned regions of 32 Arcidae mitogenomes were compared to verify the presence of these novel mitochondrial ORFs and their distribution. Strikingly, multiple structural analyses and functional prediction suggested that these additional mtDNA-encoded proteins have potential functional significance. In addition, our results also revealed that the ORFs have a strong connection to the expansion of Arcidae mitochondrial genomes and their large-scale duplication play an important role in multiple expansion events. We discussed the possible origin of ORFs and hypothesized that these ORFs may originate from duplication of mitochondrial genes.
The presence of lineage-specific mitochondrial ORFs with transcriptional activity and potential functional significance supports novel features for Arcidae mitochondrial genomes. Given our observation and analyses, these ORFs may be products of mitochondrial gene duplication. These findings shed light on the origin and function of novel mitochondrial genes in bivalves and provide new insights into evolution of mitochondrial genome size in metazoans.
贻贝科（Arcidae）包括约 260 种贻贝，是瓣鳃纲软体动物中具有重要生态和经济意义的谱系。有趣的是，几种贻贝科物种的线粒体基因组比大多数两侧对称动物的基因组大 2-3 倍，是迄今为止报道的最大的两侧对称动物线粒体基因组之一。大的线粒体基因组大小主要是由于未分配区域（功能未分配的区域）的扩张。以前对贻贝科 mtDNA 基因组未分配区域的研究主要集中在核苷酸水平的分析上，以观察序列特征，但扩张的起源仍不清楚。
我们组装了六个新的线粒体基因组并对 Scapharca broughtonii 进行了六个转录组测序，以鉴定在未分配区域转录的保守功能 ORF。从七个贻贝科物种中鉴定出了 16 个具有不同拷贝数的谱系特异性 ORF，其中 11 个 ORF 被表达并且可能具有生物活性。比较了 32 个贻贝科线粒体基因组的未分配区域，以验证这些新的线粒体 ORF 的存在及其分布。引人注目的是，多种结构分析和功能预测表明，这些额外的线粒体编码蛋白具有潜在的功能意义。此外，我们的结果还表明，这些 ORF 与贻贝科线粒体基因组的扩张密切相关，其大规模复制在多次扩张事件中发挥了重要作用。我们讨论了 ORF 的可能起源，并假设这些 ORF 可能起源于线粒体基因的复制。
具有转录活性和潜在功能意义的谱系特异性线粒体 ORF 的存在支持了贻贝科线粒体基因组的新特征。鉴于我们的观察和分析，这些 ORF 可能是线粒体基因复制的产物。这些发现揭示了双壳类动物中新的线粒体基因的起源和功能，并为后生动物线粒体基因组大小的进化提供了新的见解。
