Genus-Wide Characterization of Nuclear Mitochondrial DNAs in Bumblebee (Hymenoptera: Apidae) Genomes

Abstract

In eukaryotes, DNA of mitochondria is transferred into the nucleus and forms nuclear mitochondrial DNAs (NUMTs). Taking advantage of the abundant genomic resources for bumblebees, in this study, we de novo generated mitochondrial genomes (mitogenomes) for 11 bumblebee species. Then, we identified and characterized NUMTs in genus-wide bumblebee species. The number of identified NUMTs varies across those species, with numbers ranging from 32 to 72, and nuclear genome size is not positively related to NUMT number. The insertion sites of NUMTs in the nuclear genome are not random, with AT-rich regions harboring more NUMTs. In addition, our results suggest that NUMTs derived from the mitochondrial COX1 gene are most abundant in the bumblebee nuclear genome. Although the majority of NUMTs are found within intergenic regions, some NUMTs do reside within genic regions. Transcripts that contain both the NUMT sequence and its flanking non-NUMT sequences could be found in the bumblebee transcriptome, suggesting a potential domestication of NUMTs in the bumblebee. Taken together, our results shed light on the molecular features of NUMTs in the bumblebee and uncover their contribution to genome innovation.

The longest mitochondrial protein in metazoans is encoded by the male-transmitted mitogenome of the bivalve Scrobicularia plana

“…Scrobicularia plana [20] results in a significant enlargement of the protein: (i) the insertion does not contain any premature stop codon, it is conserved among individuals from different populations (over 300 km apart) and it bears the signature of purifying selection, which can be interpreted as a way to maintain a functional protein and (ii) the insertion is transcribed and a protein of approximately 220 kDa was detected in sperm by western blot analysis, which corresponds to the expected size of the MCOX2 peptide with the insertion. We believe that our observations are not the result of nuclear mtDNA segments (NUMTs; [39]) because (i) the complete male mitogenome of S. plana has been assembled with MITObim [20], a program expected to perform well even for species with high number of NUMTs [40], (ii) NUMTs greater than 4 kb are usually rare in animal genomes, and they are mostly non-functional pseudo-genes and rarely expressed [41][42][43], (iii) we were able to amplify large portions of Mcox2 both at the DNA and RNA levels, and (iv) the Mcox2 gene cannot be completely translated using the universal genetic code (in particular, there is no possible ORF > 50 aa using the universal genetic code for the region containing the epitope CDKYKVFPHWE specific to MCOX2 used to generate our antibody).…”

Comparison of detection methods and genome quality when quantifying nuclear mitochondrial insertions in vertebrate genomes

“…Mitochondrial and nuclear genomes have been co-evolving for more than a billion years, so that most of the proteins needed for mitochondrial function are now found in the nuclear genome following the gradual transfer of ancestral mitochondrial (mtDNA) genes to the nucleus ( du Buy and Riley, 1967 ; Lang et al, 1999 ). The transfer and insertion of mtDNA genome fragments into the nuclear genome has continued, with nuclear copies of mtDNA fragments documented in a variety of species ( Hazkani-Covo et al, 2010 ; Yan et al, 2019 ; Ding et al, 2021 ; Zhang et al, 2022 ). These nuclear insertions or “numts” ( Lopez et al, 1994 ) are widespread among eukaryotes, but despite their ubiquity, numt function is largely unknown.…”