A Burst of Numt Insertion in the Dasyuridae Family During Marsupial Evolution

Einat Hazkani-Covo

doi:10.3389/fevo.2022.844443

Abstract

Nuclear pseudogenes of mitochondrial origin (numts) are common in all eukaryotes. Our previous scan of numts in sequenced nuclear genomes suggested that the highest numt content currently known in animals is that in the gray short-tailed opossum. The present work sought to determine numt content in marsupials and to compare it to those in placental and monothematic mammals as well as in non-mammalian vertebrates. To achieve this, 70 vertebrate species with available nuclear and mitochondrial genomes were scanned for numt content. An extreme numt content was found in the Dasyuridae, with 3,450 in Sarcophilus harrisii (1,955 kb) and 2,813 in Antechinus flavipes (847 kb). The evolutionarily closest species analyzed, the extinct Thylacinus cynocephalus belonging to the Thylacindae family, had only 435 numts (238 kb). These two Dasyuridae genomes featured the highest numt content identified in animals to date. A phylogenetic analysis of numts longer than 300 bp, using a Diprotodonita mitochondrial tree, indicated a burst of numt insertion that began before the divergence of the Dasyurini and Phascogalini, reaching a peak in the early evolution of the two tribes. No comparable increase was found in the early divergent species T. cynocephalus. Divergence of the Dasyuridae tribes has been previously dated to shortly after the Miocene climate transition, characterized by a rapid temperature decline. Interestingly, deviation from optimal growth temperature is one of the environmental factors reported to increase numt insertions in a laboratory setting.

Highlights

Nuclear Pseudogenes of Mitochondrial Origin Content Varied Dramatically, With the Highest Number Found in Dasyuromorphia
In seven species of placental mammals that featured at least 100 numts, 20% or more of these were complex: Felis catus genome (31%), Papio anubis (22%), Physeter catodon (38%), and Sus scrofa (27%); in marsupials: Tursiops truncatus (39%), and the extinct Thylacinus cynocephalus (51%); and one lizard, Lacerta agilis (20%)
The current analysis sought to identify recent sequenced genomes featuring an extreme numt content, and to determine whether the high numt content previously identified in the gray short-tailed opossum is evident in other marsupials

Summary

Introduction

Mitochondria encode only a small portion of the genes (3–60) needed for mitochondrial function (Timmis et al, 2004), while the majority of mitochondrial proteins are encoded on genes in the nuclear genome and their products are targeted into the organelles (Meisinger et al, 2008; Kleine et al, 2009) This reduction in gene number encoded within the mitochondria is explained by the occurrence of endosymbiotic gene transfer (EGT): the transfer of genes from the organelle ancestor to the nuclear genome during evolution (Allen, 2015). A recent analysis of generation sequencing demonstrated that numts constitute an important component of human and primate genomic variation, both through normal evolution (Dayama et al, 2014, 2020) and through cancer dynamics (Ju et al, 2014, 2015)

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Conclusion