Gene Order in Mitochondrial DNA Affects Abundance of their Transcripts (A Case of Marine Nematodes)

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Olga V. Nikolaeva¹, Anna S. Ovcharenko^1,2, Polina V. Khorkhordina^1,2, Tatyana S. Miroliubova^1,3, Nataliya S. Sadovskaya¹, Victoria A. Scobeyeva^1,2, Nadya P. Sanamyan⁴, Elena G. Panina⁵, Kirill V. Mikhailov^1,6, Leonid Yu. Rusin⁶, Alexei V. Tchesunov^1,2, and Vladimir V. Aleoshin^1,2,6,a*

¹Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119234 Moscow, Russia

²Faculty of Biology, Lomonosov Moscow State University, 119234 Moscow, Russia

³Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071 Moscow, Russia

⁴Kamchatka Branch of the Pacific Institute of Geography, Far Eastern Branch of the Russian Academy of Sciences, 683000 Petropavlovsk-Kamchatsky, Russia

⁵Zoological Institute, Russian Academy of Sciences, 199034 Saint Petersburg, Russia

⁶Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, 127051 Moscow, Russia

^* To whom correspondence should be addressed.

Received: July 10, 2025; Revised: November 13, 2025; Accepted: November 14, 2025

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Mitochondrial genomes of most animals contain the same set of genes, with all or many protein-coding genes (PCGs) arranged in the same order, forming conserved blocks termed syntenies. Some syntenies have been preserved for hundreds of millions of years and are found in both vertebrates and invertebrates. This evolutionary conservation indicates functional role for PCG arrangement; however, biochemical and/or physiological mechanisms by which the gene order in mtDNA affects viability are unknown. Among animals, there are taxa that have completely lost conserved syntenies in mtDNA. Canonical animal syntenies in mtDNA have not been reported in nematodes, until some were recently discovered in the previously unstudied nematode taxa, including the marine family Thoracostomopsidae (Nematoda, Enoplida). We sequenced the complete mitochondrial genomes of three thoracostomopsid species, determined gene order, and their expression levels from the RNA-seq data for all available family representatives. We found that six species of the Thoracostomopsidae there are three distinct patterns of PCG arrangement, and the relative mRNA levels correlate with the gene order rather than species phylogeny. We hypothesize that the influence of PCG translocations on their expression levels underlies the long-term preservation of mitochondrial syntenies among animals.

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KEY WORDS: mtDNA, mitogenome, transcriptome, genome sequencing, RNA-seq, molecular evolution, phylogeny, nematodes, Enoplia, Thoracostomopsidae, Enoplolaimus, Marimermis, Thoracostomopsis, Trileptium

DOI: 10.1134/S0006297925602114

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