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Title: Complementing aculiferan mitogenomics: comparative characterization of mitochondrial genomes of Solenogastres (Mollusca, Aplacophora)
Abstract BackgroundWith the advances in high-throughput sequencing and bioinformatic pipelines, mitochondrial genomes have become increasingly popular for phylogenetic analyses across different clades of invertebrates. Despite the vast rise in available mitogenomic datasets of molluscs, one class of aplacophoran molluscs – Solenogastres (or Neomeniomorpha) – is still neglected. ResultsHere, we present six new mitochondrial genomes from five families of Solenogastres (Amphimeniidae, Gymnomeniidae, Proneomeniidae, Pruvotinidae, Simrothiellidae), including the first complete mitogenomes, thereby now representing three of the four traditional orders. Solenogaster mitogenomes are variable in size (ranging from approximately 15,000 bp to over 17,000 bp). The gene order of the 13 protein coding genes and two rRNA genes is conserved in three blocks, but considerable variation occurs in the order of the 22 tRNA genes. Based on phylogenetic analyses and reconstruction of ancestral mitochondrial genomes of Aculifera, the position of (1) trnD gene between atp8 and atp6, (2) trnT and P genes between atp6 and nad5, and (3) trnL1 gene between G and E, resulting in a ‘MCYWQGL1E’-block of tRNA genes, are all three considered synapomorphies for Solenogastres. The tRNA gene block ‘KARNI’ present in Polyplacophora and several conchiferan taxa is dissolved in Solenogastres. ConclusionOur study shows that mitogenomes are suitable to resolve the phylogenetic relationships among Aculifera and within Solenogastres, thus presenting a cost and time efficient compromise to approach evolutionary history in these clades. more »« less
Warren, Jessica M; Ceriotti, Luis F; Sanchez-Puerta, M Virginia; Sloan, Daniel B
(, Molecular Biology and Evolution)
Hendrickson, Heather
(Ed.)
Plant mitochondrial genomes (mitogenomes) experience remarkable levels of horizontal gene transfer, including the recent discovery that orchids anciently acquired DNA from fungal mitogenomes. Thus far, however, there is no evidence that any of the genes from this interkingdom horizontal gene transfer are functional in orchid mitogenomes. Here, we applied a specialized sequencing approach to the orchid Corallorhiza maculata and found that some fungal-derived tRNA genes in the transferred region are transcribed, post-transcriptionally modified, and aminoacylated. In contrast, all the transferred protein-coding sequences appear to be pseudogenes. These findings show that fungal horizontal gene transfer has altered the composition of the orchid mitochondrial tRNA pool and suggest that these foreign tRNAs function in translation. The exceptional capacity of tRNAs for horizontal gene transfer and functional replacement is further illustrated by the diversity of tRNA genes in the C. maculata mitogenome, which also include genes of plastid and bacterial origin in addition to their native mitochondrial counterparts.
ABSTRACT Mitochondria originated from an ancient bacterial endosymbiont that underwent reductive evolution by gene loss and endosymbiont gene transfer to the nuclear genome. The diversity of mitochondrial genomes published to date has revealed that gene loss and transfer processes are ongoing in many lineages. Most well-studied eukaryotic lineages are represented in mitochondrial genome databases, except for the superphylum Retaria—the lineage comprising Foraminifera and Radiolaria. Using single-cell approaches, we determined two complete mitochondrial genomes of Foraminifera and two nearly complete mitochondrial genomes of radiolarians. We report the complete coding content of an additional 14 foram species. We show that foraminiferan and radiolarian mitochondrial genomes contain a nearly fully overlapping but reduced mitochondrial gene complement compared to other sequenced rhizarians. In contrast to animals and fungi, many protists encode a diverse set of proteins on their mitochondrial genomes, including several ribosomal genes; however, some aerobic eukaryotic lineages (euglenids, myzozoans, and chlamydomonas-like algae) have reduced mitochondrial gene content and lack all ribosomal genes. Similar to these reduced outliers, we show that retarian mitochondrial genomes lack ribosomal protein and tRNA genes, contain truncated and divergent small and large rRNA genes, and contain only 14 or 15 protein-coding genes, including nad1 , - 3 , - 4 , - 4L , - 5 , and - 7 , cob , cox1 , - 2 , and - 3 , and atp1 , - 6 , and - 9 , with forams and radiolarians additionally carrying nad2 and nad6 , respectively. In radiolarian mitogenomes, a noncanonical genetic code was identified in which all three stop codons encode amino acids. Collectively, these results add to our understanding of mitochondrial genome evolution and fill in one of the last major gaps in mitochondrial sequence databases. IMPORTANCE We present the reduced mitochondrial genomes of Retaria, the rhizarian lineage comprising the phyla Foraminifera and Radiolaria. By applying single-cell genomic approaches, we found that foraminiferan and radiolarian mitochondrial genomes contain an overlapping but reduced mitochondrial gene complement compared to other sequenced rhizarians. An alternative genetic code was identified in radiolarian mitogenomes in which all three stop codons encode amino acids. Collectively, these results shed light on the divergent nature of the mitochondrial genomes from an ecologically important group, warranting further questions into the biological underpinnings of gene content variability and genetic code variation between mitochondrial genomes.
Osborne, Megan J; Barela_Hudgell, Megan A; Caeiro-Dias, Guilherme; Turner, Thomas F
(, Mitochondrial DNA Part B)
Macrhybopsis tetranema and Oncorhynchus gilae are fish species endemic to the Southwestern United States. We present the complete mitochondrial genomes for these species. Each genome consisted of 13 protein-coding genes, two ribosomal (rRNA) genes, 22 transfer RNA (tRNA) genes, and the control region (D-loop). Mitogenome lengths were 16,916 base pairs (bp) for M. tetranema, and 16,976 bp for O. gilae. The GC content was 41% for M. tetranema and 46% for O. gilae. The relationships of M. tetranema and O. gilae were consistent with previous phylogenetic analyses.
Lavrov, Dennis V; Turner, Thomas L; Vicente, Jan
(, bioRxiv)
<bold>Abstract</bold> Mitochondrial tRNA gene loss and cytosolic tRNA import to mitochondria are two common phenomena in mitochondrial biology, but their importance is often under-appreciated in animals. This is because most bilaterally symmetrical animals (Bilateria) encode a complete set of tRNAs needed for mitochondrial translation. By contrast, studies of mitochondrial genomes in non-bilaterian animals have shown a reduced tRNA gene content in several lineages, necessitating tRNA import. Interestingly, in most of these lineages tRNA gene content appears to be set early in the evolution of the group and conserved thereafter. Here we demonstrate that Clade B of Haplosclerid Sponges (CBHS) represent an exception to this pattern. We determined mt-genome sequences for eight species from this group and analyzed them with six that had been previously available. In addition, we determined mt-genome sequences for two species of haploslerid sponges outside the CBHS and used them with eight previously available sequences as outgroups. We found that tRNA gene content varied widely among CBHS species: from three in an undescribedHaliclonaspecies (Haliclona sp. TLT785) to 25 inXestospongia mutaandX. testudinaria. Furthermore, we found that all CBHS species outside the genusXestospongialackedatp9, while some also lackedatp8. Analysis of nuclear sequences fromNiphates digitalisrevealed that bothatp8andatp9had transferred to the nuclear genome, while the absence of mt-tRNA genes represented their genuine loss. Overall, CBHS can be a useful animal system to study mt-tRNA genes loss, mitochondrial import of cytosolic tRNA, and the impact of both of these processes on mitochondrial evolution. Significance statementIt is generally believed that the gene content is stable in animal mitochondrial (mt) DNA. Indeed, mtDNA in most bilaterally symmetrical animals encompasses a conserved set of 37 genes coding for 13 proteins, two rRNAs and 22 tRNAs. By contrast, mtDNA in non-bilaterian animals shows more variation in mt gene content, in particular in the number of tRNA genes. However, most of this variation occurs between major non-bilaterian lineages. Here we demonstrate that a group of demosponges called Clade B of Haplosclerid Sponges (CBHS) represents a fascinating exception to this pattern, with species experiencing recurrent losses of up to 22 mt-tRNA genes. We argue that this group constitutes a promising system to investigate the effects of tRNA gene loss on evolution of mt-genomes as well as mitochondrial tRNA import machinery.
Benito, Joseph B; Porter, Megan L; Niemiller, Matthew L
(, BMC Genomics)
Abstract Mitochondrial genomes play important roles in studying genome evolution, phylogenetic analyses, and species identification. Amphipods (Class Malacostraca, Order Amphipoda) are one of the most ecologically diverse crustacean groups occurring in a diverse array of aquatic and terrestrial environments globally, from freshwater streams and lakes to groundwater aquifers and the deep sea, but we have a limited understanding of how habitat influences the molecular evolution of mitochondrial energy metabolism. Subterranean amphipods likely experience different evolutionary pressures on energy management compared to surface-dwelling taxa that generally encounter higher levels of predation and energy resources and live in more variable environments. In this study, we compared the mitogenomes, including the 13 protein-coding genes involved in the oxidative phosphorylation (OXPHOS) pathway, of surface and subterranean amphipods to uncover potentially different molecular signals of energy metabolism between surface and subterranean environments in this diverse crustacean group. We compared base composition, codon usage, gene order rearrangement, conducted comparative mitogenomic and phylogenomic analyses, and examined evolutionary signals of 35 amphipod mitogenomes representing 13 families, with an emphasis on Crangonyctidae. Mitogenome size, AT content, GC-skew, gene order, uncommon start codons, location of putative control region (CR), length ofrrnLand intergenic spacers differed between surface and subterranean amphipods. Among crangonyctid amphipods, the spring-dwellingCrangonyx forbesiexhibited a unique gene order, a longnad5locus, longerrrnLandrrnSloci, and unconventional start codons. Evidence of directional selection was detected in several protein-encoding genes of the OXPHOS pathway in the mitogenomes of surface amphipods, while a signal of purifying selection was more prominent in subterranean species, which is consistent with the hypothesis that the mitogenome of surface-adapted species has evolved in response to a more energy demanding environment compared to subterranean amphipods. Overall, gene order, locations of non-coding regions, and base-substitution rates points to habitat as an important factor influencing the evolution of amphipod mitogenomes.
Bergmeier, Franziska S, Brachmann, Andreas, Kocot, Kevin M, Leasi, Francesca, Poustka, Albert J, Schrödl, Michael, Sevigny, Joseph L, Thomas, W Kelley, Todt, Christiane, and Jörger, Katharina M. Complementing aculiferan mitogenomics: comparative characterization of mitochondrial genomes of Solenogastres (Mollusca, Aplacophora). Retrieved from https://par.nsf.gov/biblio/10656639. BMC Ecology and Evolution 24.1 Web. doi:10.1186/s12862-024-02311-5.
Bergmeier, Franziska S, Brachmann, Andreas, Kocot, Kevin M, Leasi, Francesca, Poustka, Albert J, Schrödl, Michael, Sevigny, Joseph L, Thomas, W Kelley, Todt, Christiane, & Jörger, Katharina M. Complementing aculiferan mitogenomics: comparative characterization of mitochondrial genomes of Solenogastres (Mollusca, Aplacophora). BMC Ecology and Evolution, 24 (1). Retrieved from https://par.nsf.gov/biblio/10656639. https://doi.org/10.1186/s12862-024-02311-5
Bergmeier, Franziska S, Brachmann, Andreas, Kocot, Kevin M, Leasi, Francesca, Poustka, Albert J, Schrödl, Michael, Sevigny, Joseph L, Thomas, W Kelley, Todt, Christiane, and Jörger, Katharina M.
"Complementing aculiferan mitogenomics: comparative characterization of mitochondrial genomes of Solenogastres (Mollusca, Aplacophora)". BMC Ecology and Evolution 24 (1). Country unknown/Code not available: Springer. https://doi.org/10.1186/s12862-024-02311-5.https://par.nsf.gov/biblio/10656639.
@article{osti_10656639,
place = {Country unknown/Code not available},
title = {Complementing aculiferan mitogenomics: comparative characterization of mitochondrial genomes of Solenogastres (Mollusca, Aplacophora)},
url = {https://par.nsf.gov/biblio/10656639},
DOI = {10.1186/s12862-024-02311-5},
abstractNote = {Abstract BackgroundWith the advances in high-throughput sequencing and bioinformatic pipelines, mitochondrial genomes have become increasingly popular for phylogenetic analyses across different clades of invertebrates. Despite the vast rise in available mitogenomic datasets of molluscs, one class of aplacophoran molluscs – Solenogastres (or Neomeniomorpha) – is still neglected. ResultsHere, we present six new mitochondrial genomes from five families of Solenogastres (Amphimeniidae, Gymnomeniidae, Proneomeniidae, Pruvotinidae, Simrothiellidae), including the first complete mitogenomes, thereby now representing three of the four traditional orders. Solenogaster mitogenomes are variable in size (ranging from approximately 15,000 bp to over 17,000 bp). The gene order of the 13 protein coding genes and two rRNA genes is conserved in three blocks, but considerable variation occurs in the order of the 22 tRNA genes. Based on phylogenetic analyses and reconstruction of ancestral mitochondrial genomes of Aculifera, the position of (1) trnD gene between atp8 and atp6, (2) trnT and P genes between atp6 and nad5, and (3) trnL1 gene between G and E, resulting in a ‘MCYWQGL1E’-block of tRNA genes, are all three considered synapomorphies for Solenogastres. The tRNA gene block ‘KARNI’ present in Polyplacophora and several conchiferan taxa is dissolved in Solenogastres. ConclusionOur study shows that mitogenomes are suitable to resolve the phylogenetic relationships among Aculifera and within Solenogastres, thus presenting a cost and time efficient compromise to approach evolutionary history in these clades.},
journal = {BMC Ecology and Evolution},
volume = {24},
number = {1},
publisher = {Springer},
author = {Bergmeier, Franziska S and Brachmann, Andreas and Kocot, Kevin M and Leasi, Francesca and Poustka, Albert J and Schrödl, Michael and Sevigny, Joseph L and Thomas, W Kelley and Todt, Christiane and Jörger, Katharina M},
}
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