The tunicate mitochondrial genome

Genetic code

https://www.ncbi.nlm.nih.gov/Taxonomy/taxonomyhome.html/index.cgi?chapter=cgencodes#SG13

https://en.wikipedia.org/wiki/Ascidian_mitochondrial_code

                     AGA   AGG   ATA   AAA   TGA
Standard (non-mito)   R     R     I     K     *
Yeast                 R     R     M     K     W   (plus other yeast-specific changes)
Invertebrates         S     S     M     K     W
Vertebrates           *     *     M     K     W
Tunicates             G     G     M     K     W   (O. di, salps, ascidians)
 O. longicauda        G     G     I     K     ø?
 M. erythrocephalus   G     G     ø?    K     ?
 B. stygius           G     G     I     K     R
Cephalochordates      S    S,ø?   M     K     W   (standard invertebrate)
Hemichordates         S     ø     I     ø     W
Hemichordates (alt)   S     K     I     K     W   And also TAA → Y
Echinoderms           S     S     I     N     W

Genes

Transcription

Other

Mitochondria can be lost in eukaryotes, be them monocellular (Karnkowska and coll., 2019), or multicellular (Yahalomi and coll., 2020).

Mitochondrial DNA has a few rNTP misincorporated, but they do not seem to be detrimental (Wanrooij and coll., 2020).

The presence of mtDNA concatemers in nuclear genomes was postulated by Balciuniene and Balciunas (2019).

The Vertebrate Genome Project has a tool to remove NUMTs (?Rhie and coll., 2021).

Elimination of rNMPs from mitochondrial DNA has no effect on its stability.

Elimination of rNMPs from mitochondrial DNA has no effect on its stability.

Proc Natl Acad Sci U S A. 2020 Jun 23;117(25):14306-14313

Wanrooij PH, Tran P, Thompson LJ, Carvalho G, Sharma S, Kreisel K, Navarrete C, Feldberg AL, Watt DL, Nilsson AK, Engqvist MKM, Clausen AR, Chabes A.

In mouse, mitochondrial DNA strands have a few (usually ~10 or less) ribonucleotides misincorporated into them. Their number correlate with the ration between rNTPs and dNTPs. Reducing misincorporation did not have obvious benefits for the animals.

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The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion.

Karnkowska A, Treitli SC, Brzoň O, Novák L, Vacek V, Soukal P, Barlow LD, Herman EK, Pipaliya SV, Pánek T, Žihala D, Petrželková R, Butenko A, Eme L, Stairs CW, Roger AJ, Eliáš M, Dacks JB, Hampl V.

Mol Biol Evol. 2019 Oct 1;36(10):2292-2312. doi:10.1093/molbev/msz147

The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion.

Estimated genome size: ∼75 Mb; 16,768 predicted protein genes. Number of predicted introns: 31,639. Mean predicted intron length: 124.3. Telomeric repeat TTAGGG. Missing NHEJ pathway and peroxisomes.

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A cnidarian parasite of salmon (Myxozoa: Henneguya) lacks a mitochondrial genome.

Proc Natl Acad Sci U S A. 2020 Mar 10;117(10):5358-5363. doi:10.1073/pnas.1909907117

Yahalomi D, Atkinson SD, Neuhof M, Chang ES, Philippe H, Cartwright P, Bartholomew JL, Huchon D.

A cnidarian parasite of salmon (Myxozoa: Henneguya) lacks a mitochondrial genome.

The mitochondrial DNA can not be found by sequencing nor by imaging, and proteins from the respiratory chain are absent from the nuclear genome. In addition, the mitochondrial DNA polymerase is a pseudogene. The remaining mitochondria-related organelles (MROs) still have some morphological features of mitochondria, and may carry remaining biochemical pathways.

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Unusual genetic codes and a novel gene structure for tRNA(AGYSer) in starfish mitochondrial DNA.

Himeno H, Masaki H, Kawai T, Ohta T, Kumagai I, Miura K, Watanabe K.

Gene. 1987;56(2-3):219-30 doi:10.1016/0378-1119(87)90139-9

Unusual genetic codes and a novel gene structure for tRNA(AGYSer) in starfish mitochondrial DNA.

AGA and AGG code for serine as in the main invertebrate mitochondrial code, but AUA codes for isoleucine and AAA for asparagine.

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The mitochondrial genome of the hemichordate Balanoglossus carnosus and the evolution of deuterostome mitochondria.

Genetics. 1998 Nov;150(3):1115-23.

Castresana J, Feldmaier-Fuchs G, Yokobori S, Satoh N, Pääbo S.

The mitochondrial genome of the hemichordate Balanoglossus carnosus and the evolution of deuterostome mitochondria.

AGA encodes Ser, AGG is absent, ATA encodes Ile, AAA is absent. “…out of the 69 ATA hemichordate codons, 20 occur in positions where Ile is conserved in >55% of the sequences (eight of these positions have Ile in >90% of the sequences), while none of them occur at positions where Met is conserved. Of the 19 AGA codons, 6 occur at positions where Ser is conserved in >55% of the sequences (3 of them with Ser in >90% of the sequences), whereas they are never used as stop codons.”

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Complete mtDNA of Ciona intestinalis reveals extensive gene rearrangement and the presence of an atp8 and an extra trnM gene in ascidians.

J Mol Evol. 2004 Apr;58(4):376-89 doi:10.1007/s00239-003-2559-6

Gissi C, Iannelli F, Pesole G.

Complete mtDNA of Ciona intestinalis reveals extensive gene rearrangement and the presence of an atp8 and an extra trnM gene in ascidians.

Gene order varies even within the Ciona genus. A short atp8 gene is found in Ciona and Halocynthia.

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Nucleotide sequence of cytochrome oxidase (subunit III) from the mitochondrion of the tunicate Pyura stolonifera: evidence that AGR encodes glycine.

Durrheim GA, Corfield VA, Harley EH, Ricketts MH.

Nucleic Acids Res. 1993 Jul 25;21(15):3587-8.

Nucleotide sequence of cytochrome oxidase (subunit III) from the mitochondrion of the tunicate Pyura stolonifera: evidence that AGR encodes glycine.

AGR -> Gly in another tunicate. Protein tranlated assuming ATA -> Met and TGA -> Trp like in vertebrates and invertebrates.

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Tunicate mitogenomics and phylogenetics: peculiarities of the Herdmania momus mitochondrial genome and support for the new chordate phylogeny

Tiratha Raj Singh, Georgia Tsagkogeorga, Frédéric Delsuc, Samuel Blanquart, Noa Shenkar, Yossi Loya, Emmanuel JP Douzery and Dorothée Huchon

BMC Genomics. 2009 Nov 17;10:534. doi: 10.1186/1471-2164-10-534

Tunicate mitogenomics and phylogenetics: peculiarities of the Herdmania momus mitochondrial genome and support for the new chordate phylogeny

The cox2-cytb pair, usually found in tunicates, is separated in the solitary ascidian Herdmania momus.

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One tunic but more than one barcode: evolutionary insights from dynamic mitochondrial DNA in Salpa thompsoni (Tunicata: Salpida)

William P. Goodall-Copestake

Biological Journal of the Linnean Society, Volume 120, Issue 3, 1 March 2017, Pages 637–648, https://doi.org/10.1111/bij.12915

One tunic but more than one barcode: evolutionary insights from dynamic mitochondrial DNA in Salpa thompsoni (Tunicata: Salpida)

Found ”inverse PCR amplicons [that] could occur in vivo as single circular DNAs and/or as tandem repeats within a larger circular or linear molecule”

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UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota.

Proc Natl Acad Sci U S A. 2013 Apr 2;110(14):5540-5. doi:10.1073/pnas.1303090110

Campbell JH, O'Donoghue P, Campbell AG, Schwientek P, Sczyrba A, Woyke T, Söll D, Podar M.

UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota.

“Coexpression of SR1 glycyl-tRNA synthetase and tRNA(Gly)UCA in Escherichia coli yields significant β-galactosidase activity in vivo from a lacZ gene containing an in-frame TGA codon.”

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The main features of the craniate mitochondrial DNA between the ND1 and the COI genes were established in the common ancestor with the lancelet.

Mol Biol Evol. 1997 Aug;14(8):807-13 doi:10.1093/oxfordjournals.molbev.a025821

Delarbre C, Barriel V, Tillier S, Janvier P, Gachelin G.

The main features of the craniate mitochondrial DNA between the ND1 and the COI genes were established in the common ancestor with the lancelet.

Proposes AGR -> Gly based on AGG / GGG polymorphisms in the population.

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Complete sequence, gene arrangement, and genetic code of mitochondrial DNA of the cephalochordate Branchiostoma floridae (Amphioxus)

Mol Biol Evol. 1999 Mar;16(3):410-8 doi:10.1093/oxfordjournals.molbev.a026122

Boore JL, Daehler LL, Brown WM.

Complete sequence, gene arrangement, and genetic code of mitochondrial DNA of the cephalochordate Branchiostoma floridae (Amphioxus)

AGA encodes serine in amphioxus mitochondrial DNA. AGG is absent. AGA and AGG are reduced in frequencey compared to the AGY serine codons, which suggests a that the common ancestor of chordates had a precondition for AGR reassignment.

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Complete sequence of the amphioxus (Branchiostoma lanceolatum) mitochondrial genome: relations to vertebrates.

Spruyt N, Delarbre C, Gachelin G, Laudet V.

Nucleic Acids Res. 1998 Jul 1;26(13):3279-85 doi:10.1093/nar/26.13.3279

Complete sequence of the amphioxus (Branchiostoma lanceolatum) mitochondrial genome: relations to vertebrates.

AGA translated to Gly as in tunicates. Found a possible 23rd tRNA, with a TCT (Gly) anticodon. AGG is not used.

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Complete DNA sequence of the mitochondrial genome of the ascidian Halocynthia roretzi (Chordata, Urochordata).

Genetics. 1999 Dec;153(4):1851-62

Yokobori Si, Ueda T, Feldmaier-Fuchs G, Pääbo S, Ueshima R, Kondow A, Nishikawa K, Watanabe K.

Complete DNA sequence of the mitochondrial genome of the ascidian Halocynthia roretzi (Chordata, Urochordata).

The nucleotide sequence of Halocynthia mtDNA has been deposited in the DDBJ/GenBank/EMBL DNA databases under the accession no. AB024528

Sequence of the Halocynthia roretzi mitochondrial genome. Gene order strongly differs from vertebrates. The predicted novel tRNAGly is found.

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Codon reassignment and amino acid composition in hemichordate mitochondria.

Jose Castresana, Gertraud Feldmaier-Fuchs, and Svante Pääbo

Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3703-7 doi:10.1073/pnas.95.7.3703

“In the mitochondrial genome of the hemichordate Balanoglossus carnosus, the codon AAA, which is assigned to lysine in most metazoans but to asparagine in echinoderms, is absent. Furthermore, the lysine tRNA gene carries an anticodon substitution that renders its gene product unable to decode AAA codons, whereas the asparagine tRNA gene has not changed to encode a tRNA with the ability to recognize AAA codons. Thus, the hemichordate mitochondrial genome can be regarded as an intermediate in the process of reassignment of mitochondrial AAA codons, where most metazoans represent the ancestral situation and the echinoderms the derived situation. This lends support to the codon capture hypothesis.”

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Codons AGA and AGG are read as glycine in ascidian mitochondria.

J Mol Evol. 1993 Jan;36(1):1-8. doi:10.1007/BF02407301

Yokobori S, Ueda T, Watanabe K.

Codons AGA and AGG are read as glycine in ascidian mitochondria.

Analysis of Halocynthia roretzi Cox1 cDNA sequence suggests that in the ascidian mitochondrial genetic code, AGR code for Gly (unlike other animals), ATA for Met (like vertebrates and invertebrates) and TGA for Trp (like vertebrates and invertebrates).

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Mitochondrial genome of Ciona savignyi (Urochordata, Ascidiacea, Enterogona): comparison of gene arrangement and tRNA genes with Halocynthia roretzi mitochondrial genome.

J Mol Evol. 2003 Nov;57(5):574-87 doi: 10.1007/s00239-003-2511-9

Yokobori S, Watanabe Y, Oshima T.

Mitochondrial genome of Ciona savignyi (Urochordata, Ascidiacea, Enterogona): comparison of gene arrangement and tRNA genes with Halocynthia roretzi mitochondrial genome.

The DDBJ accession number of complete nucleotide sequence of the Ciona mtDNA is AB079784.

“The atp8 gene is absent.” “The Ciona mt genome uses the same codon table as the Halocynthia mt genome: AUA specifies Met, UGA specifies Trp, and AGA/AGG specify Gly.” “To predict the genetic code used in the Ciona mt genome, the well-conserved cox1 sequence was compared between Ciona and several other metazoans.” “The Ciona mtDNA is extremely (77.3%) AT-rich.”

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The mitochondrial genome of Phallusia mammillata and Phallusia fumigata (Tunicata, Ascidiacea): high genome plasticity at intra-genus level.

Iannelli F, Griggio F, Pesole G, Gissi C.

BMC Evol Biol. 2007 Aug 31;7:155 doi:10.1186/1471-2148-7-155

The mitochondrial genome of Phallusia mammillata and Phallusia fumigata (Tunicata, Ascidiacea): high genome plasticity at intra-genus level.

The complete mtDNA sequences of P. mammillata and P. fumigata were deposited at EMBL database under accession numbers AM292320 and AM292602, respectively.

“Sequence similarities between NC of the same mtDNA have been found in P. fumigata.” “The cox2-cob is conserved in all tunicates, probably because of an ORF overlap.”

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Absence of evidence is not evidence of absence: Nanopore sequencing and complete assembly of the European lobster (Homarus gammarus) mitogenome uncovers the missing nad2 and a new major gene cluster duplication.

Gan HM, Grandjean F, Jenkins TL, Austin CM.

BMC Genomics. 2019 May 3;20(1):335. doi: 10.1186/s12864-019-5704-3.

Absence of evidence is not evidence of absence: Nanopore sequencing and complete assembly of the European lobster (Homarus gammarus) mitogenome uncovers the missing nad2 and a new major gene cluster duplication.

Canu assembly after collecting reads matching an illumina-assembled draft genome.

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Assembly of a Complete Mitogenome of Chrysanthemum nankingense Using Oxford Nanopore Long Reads and the Diversity and Evolution of Asteraceae Mitogenomes.

Wang S, Song Q, Li S, Hu Z, Dong G, Song C, Huang H, Liu Y.

Genes (Basel). 2018 Nov 12;9(11). pii: E547. doi:10.3390/genes9110547

Assembly of a Complete Mitogenome of Chrysanthemum nankingense Using Oxford Nanopore Long Reads and the Diversity and Evolution of Asteraceae Mitogenomes.

“For the assembly using the ONT-only assembly method, the mitochondrial long reads were firstly filtered from the total ONT sequencing data using BWA v0.7.16 and SAMtools v1.9 using the contig of hybrid assembly as the reference. Then, an ONT-only assembly was generated using Canu v1.7.”

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Two reads to rule them all: Nanopore long read-guided assembly of the iconic Christmas Island red crab, Gecarcoidea natalis (Pocock, 1888), mitochondrial genome and the challenges of AT-rich mitogenomes.

Gan HM, Linton SM, Austin CM.

Mar Genomics. 2019 Mar 27. pii: S1874-7787(18)30218-6. doi:10.1016/j.margen.2019.02.002

Two reads to rule them all: Nanopore long read-guided assembly of the iconic Christmas Island red crab, Gecarcoidea natalis (Pocock, 1888), mitochondrial genome and the challenges of AT-rich mitogenomes.

9 Nanopore reads were identified by alignment to reference mitochondrial sequences with mimimap2, and then used for hybrid assembly.

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de novo assembly and population genomic survey of natural yeast isolates with the Oxford Nanopore MinION sequencer.

Istace B, Friedrich A, d'Agata L, Faye S, Payen E, Beluche O, Caradec C, Davidas S, Cruaud C, Liti G, Lemainque A, Engelen S, Wincker P, Schacherer J, Aury JM.

Gigascience. 2017 Feb 1;6(2):1-13. doi:10.1093/gigascience/giw018

de novo assembly and population genomic survey of natural yeast isolates with the Oxford Nanopore MinION sequencer.

Assembled mitochondrial genomes with ABruijn.

Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species.

Heredity (Edinb). 2008 Oct;101(4):301-20. doi:10.1038/hdy.2008.62

Gissi C, Iannelli F, Pesole G.

Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species.

Mitochondrial genomes of tunicates have all genes colinear on the same strand, and usually encode 24 tRNAs (instead of 22 in vertebrates). Their rRNA genes are separated.

Experimental evidence that thermal selection shapes mitochondrial genome evolution.

Sci Rep. 2018 Jun 22;8(1):9500. doi:10.1038/s41598-018-27805-3

Lajbner Z, Pnini R, Camus MF, Miller J, Dowling DK.

Experimental evidence that thermal selection shapes mitochondrial genome evolution.

Experimental evidence for the “mitochondrial climatic hypothesis”. Haplotypes only differ by non-coding or synonymous changes. Wolbachia infection was a confounding factor and needed to be removed by antibiotic treatment.

Identification of Transcriptional and Metabolic Programs Related to Mammalian Cell Size.

Miettinen TP, Pessa HK, Caldez MJ, Fuhrer T, Diril MK, Sauer U, Kaldis P, Björklund M.

Curr Biol. 2014 Mar 4. pii: S0960-9822(14)00136-5. doi:10.1016/j.cub.2014.01.071

Identification of Transcriptional and Metabolic Programs Related to Mammalian Cell Size.

In cells enlarged by Cdk1 knockout and partial hepatectomy, AMP levels are reduced and SREBP1 and 2 are down-regulated.

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