Fragmentation in mitochondrial genomes in relation to elevated sequence divergence and extreme rearrangements

Background A single circular mitochondrial (mt) genome is a common feature across most metazoans. The mt-genome includes protein-coding genes involved in oxidative phosphorylation, as well as RNAs necessary for translation of mt-RNAs, whose order and number are highly conserved across animal clades, with few known exceptions of alternative mt-gene order or mt-genome architectures. One such exception consists of the fragmented mitochondrial genome, a type of genome architecture where mt-genes are split across two or more mt-chromosomes. However, the origins of mt-genome fragmentation and its effects on mt-genome evolution are unknown. Here, we investigate these origin and potential mechanisms underlying mt-genome fragmentation, focusing on a genus of booklice, Liposcelis, which exhibits elevated sequence divergence, frequent rearrangement of mt-gene order, and fragmentation of the mt genome, and compare them to other Metazoan clades. Results We found this genus Liposcelis exhibits very low conservation of mt-gene order across species, relative to other metazoans. Levels of gene order rearrangement were, however, unrelated to whether or not mt-genomes were fragmented or intact, suggesting mitochondrial genome fragmentation is not affecting mt-gene order directly. We further investigated possible mechanisms underpinning these patterns and revealed very high conservation of non-coding sequences at the edges of multiple recombination regions across populations of one particular Liposcelis species, supportive of a hypothesis that mt-fragmentation arises from recombination errors between mt-genome copies. We propose these errors may arise as a consequence of a heightened mutation rate in clades exhibiting mt-fragmentation. Consistent with this, we observed a striking pattern across three Metazoan phyla (Arthropoda, Nematoda, Cnidaria) characterised by members exhibiting high levels of mt-gene order rearrangement and cases of mt-fragmentation, whereby the mt-genomes of species more closely related to species with fragmented mt-genomes diverge more rapidly despite experiencing strong purifying selection. Conclusions We showed that contrary to expectations, mt-genome fragmentation is not correlated with the increase in mt-genome rearrangements. Furthermore, we present evidence that fragmentation of the mt-genome may be part of a general relaxation of a natural selection on the mt-genome, thus providing new insights into the origins of mt-genome fragmentation and evolution.

Comparative Mitogenomics of Fungal Species in Stachybotryaceae Provides Evolutionary Insights into Hypocreales

Stachybotrys chartarum is one of the world’s ten most feared fungi within the family Stachybotryaceae, although to date, not a single mitogenome has been documented for Stachybotryaceae. Herein, six mitogenomes of four different species in Stachybotryaceae are newly reported. The S. chartarum mitogenome was 30.7 kb in length and contained two introns (one each in rnl and cox1). A comparison of the mitogenomes of three different individuals of S. chartarum showed few nucleotide variations and conservation of gene content/order and intron insertion. A comparison of the mitogenomes of four different Stachybotryaceae species (Memnoniella echinata, Myrothecium inundatum, S. chartarum, and S. chlorohalonata), however, revealed variations in intron insertion, gene order/content, and nad2/nad3 joining pattern. Further investigations on all Hypocreales species with available mitogenomes showed greater variabilities in gene order (six patterns) and nad2/nad3 joining pattern (five patterns) although a dominant pattern always existed in each case. Ancestral state estimation showed that in each case the dominant pattern was always more ancestral than those rare patterns. Phylogenetic analyses based on mitochondrion-encoded genes supported the placement of Stachybotryaceae in Hypocreales. The crown age of Stachybotryaceae was estimated to be approximately the Early Cretaceous (141–142 Mya). This study greatly promotes our understanding of the evolution of fungal species in Hypocreales.

Initial Phylotranscriptomic Confirmation of Homoplastic Evolution of the Conspicuous Coloration and Bufoniform Morphology of Pumpkin-Toadlets in the Genus Brachycephalus

The genus Brachycephalus is a fascinating group of miniaturized anurans from the Brazilian Atlantic Forest, comprising the conspicuous, brightly colored pumpkin-toadlets and the cryptic flea-toads. Pumpkin-toadlets are known to contain tetrodotoxins and therefore, their bright colors may perform an aposematic function. Previous studies based on a limited number of mitochondrial and nuclear-encoded markers supported the existence of two clades containing species of pumpkin-toadlet phenotype, but deep nodes remained largely unresolved or conflicting between data sets. We use new RNAseq data of 17 individuals from nine Brachycephalus species to infer their evolutionary relationships from a phylogenomic perspective. Analyses of almost 5300 nuclear-encoded ortholog protein-coding genes and full mitochondrial genomes confirmed the existence of two separate pumpkin-toadlet clades, suggesting the convergent evolution (or multiple reversals) of the bufoniform morphology, conspicuous coloration, and probably toxicity. In addition, the study of the mitochondrial gene order revealed that three species (B. hermogenesi, B. pitanga, and B. rotenbergae) display translocations of different tRNAs (NCY and CYA) from the WANCY tRNA cluster to a position between the genes ATP6 and COIII, showing a new mitochondrial gene order arrangement for vertebrates. The newly clarified phylogeny suggests that Brachycephalus has the potential to become a promising model taxon to understand the evolution of coloration, body plan and toxicity. Given that toxicity information is available for only few species of Brachycephalus, without data for any flea-toad species, we also emphasize the need for a wider screening of toxicity across species, together with more in-depth functional and ecological study of their phenotypes.

The Mitochondrial Genomes of 18 New Pleurosticti (Coleoptera: Scarabaeidae) Exhibit a Novel trnQ-NCR-trnI-trnM Gene Rearrangement and Clarify Phylogenetic Relationships of Subfamilies within Scarabaeidae

The availability of next-generation sequencing (NGS) in recent years has facilitated a revolution in the availability of mitochondrial (mt) genome sequences. The mt genome is a powerful tool for comparative studies and resolving the phylogenetic relationships among insect lineages. The mt genomes of phytophagous scarabs of the subfamilies Cetoniinae and Dynastinae were under-represented in GenBank. Previous research found that the subfamily Rutelinae was recovered as a paraphyletic group because the few representatives of the subfamily Dynastinae clustered into Rutelinae, but the subfamily position of Dynastinae was still unclear. In the present study, we sequenced 18 mt genomes from Dynastinae and Cetoniinae using next-generation sequencing (NGS) to re-assess the phylogenetic relationships within Scarabaeidae. All sequenced mt genomes contained 37 sets of genes (13 protein-coding genes, 22 tRNAs, and two ribosomal RNAs), with one long control region, but the gene order was not the same between Cetoniinae and Dynastinae species. All mt genomes of Dynastinae species showed the same gene rearrangement of trnQ-NCR-trnI-trnM, whereas all mt genomes of Cetoniinae species showed the ancestral insect gene order of trnI-trnQ-trnM. Phylogenetic analyses (IQ-tree and MrBayes) were conducted using 13 protein-coding genes based on nucleotide and amino acid datasets. In the ML and BI trees, we recovered the monophyly of Rutelinae, Cetoniinae, Dynastinae, and Sericinae, and the non-monophyly of Melolonthinae. Cetoniinae was shown to be a sister clade to (Dynastinae + Rutelinae).

Different gene rearrangements of the genus Dardanus (Anomura: Diogenidae) and insights into the phylogeny of Paguroidea

Complete mitochondrial genomes (mitogenomes) can provide useful information for phylogenetic relationships, gene rearrangement, and molecular evolution. In this study, the complete mitogenomes of two hermit crabs, Dardanus arrosor and Dardanus aspersus, were sequenced for the first time and compared with other published mitogenomes of Paguroidea. Each of the two mitogenomes contains an entire set of 37 genes and a putative control region, but they display different gene arrangements. The different arrangements of the two mitogenomes might be the result of transposition, reversal, and tandem duplication/random loss events from the ancestral pancrustacean pattern. Genome sequence similarity analysis reveals the gene rearrangement in 15 Paguroidea mitogenomes. After synteny analysis between the 15 Paguroidea mitogenomes, an obvious rearranged region is found in D. aspersus mitogenome. Across the 13 protein-coding genes (PCGs) tested, COI has the least and ND6 has the largest genetic distances among the 15 hermit crabs, indicating varied evolution rates of PCGs. In addition, the dN/dS ratio analysis shows that all PCGs are evolving under purifying selection. The phylogenetic analyses based on both gene order and sequence data present the monophyly of three families (Paguridae, Coenobitidae, and Pylochelidae) and the paraphyly of the family Diogenidae. Meanwhile, the phylogenetic tree based on the nucleotide sequences of 13 PCGs shows that two Dardanus species formed a sister group with five Coenobitidae species. These findings help to better understand the gene rearrangement and phylogeny of Paguroidea, as well as provide new insights into the usefulness of mitochondrial gene order as a phylogenetic marker.

Genome Comparisons of the Fission Yeasts Reveal Ancient Collinear Loci Maintained by Natural Selection

Fission yeasts have a unique life history and exhibit distinct evolutionary patterns from other yeasts. Besides, the species demonstrate stable genome structures despite the relatively fast evolution of their genomic sequences. To reveal what could be the reason for that, comparative genomic analyses were carried out. Our results provided evidence that the structural and sequence evolution of the fission yeasts were correlated. Moreover, we revealed ancestral locally collinear blocks (aLCBs), which could have been inherited from their last common ancestor. These aLCBs proved to be the most conserved regions of the genomes as the aLCBs contain almost eight genes/blocks on average in the same orientation and order across the species. Gene order of the aLCBs is mainly fission-yeast-specific but supports the idea of filamentous ancestors. Nevertheless, the sequences and gene structures within the aLCBs are as mutable as any sequences in other parts of the genomes. Although genes of certain Gene Ontology (GO) categories tend to cluster at the aLCBs, those GO enrichments are not related to biological functions or high co-expression rates, they are, rather, determined by the density of essential genes and Rec12 cleavage sites. These data and our simulations indicated that aLCBs might not only be remnants of ancestral gene order but are also maintained by natural selection.

Complete Mitochondrial Genome of Phoneutria Boliviensis (Araneae, Ctenidae): New Insights Into the Phylogeny and Evolution of Spider

Spiders are the most abundant land predators and megadiverse on earth. In recent years, the mitochondrial genome has been sequenced, mainly for ecological and commercial purposes, reporting some level of rearrangements in this genome. However, there is poor genetic information in several taxonomic families of spiders. The aim of this study was to obtain the sequence of the complete genome of Phoneutria boliviensis and, based on this, extract the mitogenomes of other species of the family Ctenidae from published transcriptomes to perform a comparative study among spider species to determine the relationship between the level of mitochondrial rearrangement and its possible relationship with molecular variability in spiders. Complete mitochondrial genomes of eighteen spiders (including nine Ctenidae species) were obtained by two different methodologies (sequencing and transcriptome extraction). Fifty-eight spider mitochondrial genomes were downloaded from the NCBI database for gene order analysis. After verifying the annotation of each mitochondrial gene, a phylogeny and gene order, analysis from 76 spider mitochondrial genomes was obtained. Our results show a high rate of annotation error in the mitochondrial genomes of spiders published in databases, which could lead to false phylogenetic relationships. Moreover, to provide new mitochondrial genomes in spiders by two different methodologies to obtain them, our analysis identifies six different mitochondrial architectures among all spiders. Translocation or tandem duplication random loss (TDRL) events in tRNA genes were identified to explain the evolution of the spider mitochondrial genome. In addition, our findings provide new insights into spider mitochondrial evolution.

The bowfin genome illuminates the developmental evolution of ray-finned fishes

The bowfin (Amia calva) is a ray-finned fish that possesses a unique suite of ancestral and derived phenotypes, which are key to understanding vertebrate evolution. The phylogenetic position of bowfin as a representative of neopterygian fishes, its archetypical body plan and its unduplicated and slowly evolving genome make bowfin a central species for the genomic exploration of ray-finned fishes. Here we present a chromosome-level genome assembly for bowfin that enables gene-order analyses, settling long-debated neopterygian phylogenetic relationships. We examine chromatin accessibility and gene expression through bowfin development to investigate the evolution of immune, scale, respiratory and fin skeletal systems and identify hundreds of gene-regulatory loci conserved across vertebrates. These resources connect developmental evolution among bony fishes, further highlighting the bowfin’s importance for illuminating vertebrate biology and diversity in the genomic era.