Skip to main content
Log in

Comparative mitogenomics of Brachiopods reveals conservatism in articulate species and unusualness in inarticulate species

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

Brachiopods are a phylum of marine invertebrates with over 10,000 fossil species. Today, there are fewer than 500 extant species assigned to the class Articulata or Inarticulata and for which knowledge of evolutionary genetics and genomics is still poor. Until now, complete mitogenome sequences of two inarticulate species and four articulate species were available.

Methods and Results

The complete mitogenome of the inarticulate brachiopod species Lingula reevii (20,778 bp) was obtained by using next generation sequencing. It contains 12 protein-coding genes (the annotation of atp8 is unsure), two ribosomal RNA genes, 26 transfer RNA genes, and one supernumerary ORF that is also conserved in the inarticulate species Lingula anatina. It is hypothesized that this ORF could represent a Lingula-specific mtORFan gene (without obvious homology to other genes). Comparative mitogenomics indicate the mitochondrial gene order of L. reevii is unique among brachiopods, and that compared to articulate species, inarticulate species exhibit massive mitogenome rearrangements, deviant ATP8 protein sequences and supernumerary ORFs, possibly representing species- or lineage-specific mtORFan genes.

Conclusion

The results of this study enrich genetics knowledge of extant brachiopods, which may eventually help to test hypotheses about their decline.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The mitochondrial genome sequence is available from the NCBI GenBank database under accession number OR906209.

References

  1. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716. https://doi.org/10.1016/j.tig.2003.10.012

    Article  PubMed  CAS  Google Scholar 

  2. Boore JL (1999) Animal mitochondrial genomes. Nucl Acids Res 27:1767–1780

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Breton S, Milani L, Ghiselli F, Guerra D, Stewart DT, Passamonti M (2014) A resourceful genome: updating the functional repertoire and evolutionary role of animal mitochondrial DNAs. Trends Genet 30:555–564

    Article  PubMed  CAS  Google Scholar 

  4. Lavrov DV, Pett W (2016) Animal mitochondrial DNA as we do not know it: mt-Genome organization and evolution in nonbilaterian lineages. Genome Biol Evol 8:2896–2913. https://doi.org/10.1093/gbe/evw195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Ghiselli F, Gomes-Dos-Santos A, Adema CM, Lopes-Lima M, Sharbrough J, Boore JL (2021) Molluscan mitochondrial genomes break the rules. Phil Trans R Soc Lond B Biol Sci 376:20200159. https://doi.org/10.1098/rstb.2020.0159

    Article  Google Scholar 

  6. Gibson T, Blok VC, Dowton M (2007) Sequence and characterization of six mitochondrial subgenomes from Globodera rostochiensis: multipartite structure is conserved among close nematode relatives. J Mol Evol 65:308–315. https://doi.org/10.1007/s00239-007-9007-y

    Article  ADS  PubMed  CAS  Google Scholar 

  7. Sultana T, Kim J, Lee SH, Han H, Kim S, Min GS, Nadler SA, Park JK (2013) Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes. BMC Evol Biol 13:12. https://doi.org/10.1186/1471-2148-13-12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Feng S, Pozzi A, Stejskal V, Opit G, Yang Q, Shao R, Dowling DK, Li Z (2022) Fragmentation in mitochondrial genomes in relation to elevated sequence divergence and extreme rearrangements. BMC Biol 20:7. https://doi.org/10.1186/s12915-021-01218-7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Yuan Y, Li Q, Yu H, Kong L (2012) The complete mitochondrial genomes of six heterodont bivalves (Tellinoidea and Solenoidea): variable gene arrangements and phylogenetic implications. PLoS ONE 7:e32353. https://doi.org/10.1371/journal.pone.0032353

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  10. McCartney MA, Auch B, Kono T, Mallez S, Zhang Y, Obille A, Becker A, Abrahante JE, Garbe J, Badalamenti JP, Herman A, Mangelson H, Liachko I, Sullivan S, Sone ED, Koren S, Silverstein KAT, Beckman KB, Gohl DM (2022) The genome of the zebra mussel, Dreissena polymorpha: a resource for comparative genomics, invasion genetics, and biocontrol. G3 (Bethesda). https://doi.org/10.1093/g3journal/jkab423

    Article  PubMed  Google Scholar 

  11. Tassé M, Choquette T, Angers A, Stewart DT, Pante E, Breton S (2022) The longest mitochondrial protein in metazoans is encoded by the male-transmitted mitogenome of the bivalve Scrobicularia plana. Biol Lett. https://doi.org/10.1098/rsbl.2022.0122

    Article  PubMed  PubMed Central  Google Scholar 

  12. Lubośny M, Śmietanka B, Lasota R, Burzyński A (2022) Confirmation of the first intronic sequence in the bivalvian mitochondrial genome of Macoma balthica (Linnaeus, 1758). Biol Lett 18:20220275. https://doi.org/10.1098/rsbl.2022.0275

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Helfenbein KG, Brown WM, Boore JL (2001) The complete mitochondrial genome of the of the articulate brachiopod Terebratalia transversa. Mol Biol Evol 18:1734–1744

    Article  PubMed  CAS  Google Scholar 

  14. Endo K, Noguchi Y, Ueshima R, Jacobs HT (2005) Novel repetitive structures, deviant protein-encoding sequences and unidentified ORFs in the mitochondrial genome of the brachiopod Lingula anatina. J Mol Evol 61:36–53

    Article  ADS  PubMed  CAS  Google Scholar 

  15. Luo Y-J, Satoh M, Endo K (2015) Mitochondrial gene order variation in the brachiopod Lingula anatina and its implications for mitochondrial evolution in lophotrochozoans. Mar Genomics 1:31–40

    Article  Google Scholar 

  16. Karagozlu MZ, Kim S-G, Thinh DD, Kim C-B (2017) Complete mitochondrial genome analysis of Lingula anatina from Korea (Brachiopoda, Lingulida, Lingulidae). Mitocondrial DNA B 2:829–830

    Article  Google Scholar 

  17. Niaison T, Guerra D, Breton S (2021) The complete mitogenome of the inarticulate brachiopod Glottidia pyramidata reveals insights into gene order variation, deviant ATP8 and mtORFans in the Brachiopoda. Mitochondrial DNA B 6:2701–2703. https://doi.org/10.1080/23802359.2021.1966342

    Article  Google Scholar 

  18. Carlson SJ (2016) The evolution of Brachiopoda. Annu Rev Earth Planet Sci 44:409–438

    Article  ADS  CAS  Google Scholar 

  19. Karagozlu MZ, Do TD, Kim JI, Choi TJ, Kim SG, Kim CB (2021) An investigation of the variations in complete mitochondrial genomes of Lingula anatina in the Western Pacific Region. Biology (Basel) 10:367. https://doi.org/10.3390/biology10050367

    Article  PubMed  CAS  Google Scholar 

  20. Stechmann A, Schlegel M (1999) Analysis of the complete mitochondrial DNA sequence of the brachiopod Terebratulina retusa places Brachiopoda within the protostomes. Proc Ro Soc Lond B 266:2043–2052

    Article  CAS  Google Scholar 

  21. Noguchi Y, Endo K, Tajima F, Ueshima R (2000) The mitochondrial genome of the brachiopod Laqueus rubellus. Genetics 155:245–259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Karagozlu MZ, Kim S-G, Thinh DD, Kim C-B (2017) Complete mitochondrial genome of Laqueus japonicus (Brachiopoda, Terebratulida, Laqueidae). Mitochondrial DNA B 2:883–884

    Article  Google Scholar 

  23. Breton S, Ghiselli F, Milani L (2021) Mitochondrial short-term plastic responses and long-term evolutionary dynamics in animal species. Genome Biol Evol. https://doi.org/10.1093/gbe/evab084

    Article  PubMed  PubMed Central  Google Scholar 

  24. Park E, Song JI, Won YJ (2011) The complete mitochondrial genome of calicogorgia granulosa (Anthozoa: Octocorallia): potential gene novelty in unidentified ORFs formed by repeat expansion and segmental duplication. Gene 486:81–87. https://doi.org/10.1016/j.gene.2011.07.003

    Article  PubMed  CAS  Google Scholar 

  25. Kayal E, Bentlage B, Collins AG, Kayal M, Pirro S, Lavrov DV (2012) Evolution of linear mitochondrial genomes in medusozoan cnidarians. Genome Biol Evol 4:1–12. https://doi.org/10.1093/gbe/evr123

    Article  PubMed  CAS  Google Scholar 

  26. Schultz DT, Eizenga JM, Corbett-Detig RB, Francis WR, Christianson LM, Haddock SHD (2020) Conserved novel ORFs in the mitochondrial genome of the ctenophore Beroe forskalii. PeerJ 8:e8356. https://doi.org/10.7717/peerj.8356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Selifanova M, Demianchenko O, Noskova E, Pitikov E, Skvortsov D, Drozd J, Vatolkina N, Apel P, Kolodyazhnaya E, Ezhova MA, Tzetlin AB, Neretina TV, Knorre DA (2023) ORFans in mitochondrial genomes of marine polychaete polydora. Genome Biol Evol. https://doi.org/10.1093/gbe/evad219

    Article  PubMed  PubMed Central  Google Scholar 

  28. Breton S, Stewart DT, Shepardson S, Trdan RJ, Bogan AE, Chapman EG, Ruminas AJ, Piontkivska H, Hoeh WR (2011) Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)? Mol Biol Evol 28:1645–1659. https://doi.org/10.1093/molbev/msq345

    Article  PubMed  CAS  Google Scholar 

  29. Milani L, Ghiselli F, Maurizii MG, Nuzhdin SV, Passamonti M (2014) Paternally transmitted mitochondria express a new gene of potential viral origin. Genome Biol Evol 6:391–405. https://doi.org/10.1093/gbe/evu021

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Ouimet P, Kienzle L, Lubosny M, Burzyński A, Angers A, Breton S (2020) The ORF in the control region of the female-transmitted Mytilus mtDNA codes for a protein. Gene 725:144161. https://doi.org/10.1016/j.gene.2019.144161

    Article  PubMed  CAS  Google Scholar 

  31. Debelli A, Kienzle L, Khorami HH, Angers A, Breton S (2030) Validation of the male-specific ORF of the paternally-transmitted mtDNA in Mytilus edulis as a protein-coding gene. Gene. https://doi.org/10.1016/j.gene.2023.147586.

  32. Zhang N, Li Y, Halanych KM, Kong L, Li Q (2022) A comparative analysis of mitochondrial ORFs provides new insights on expansion of mitochondrial genome size in Arcidae. BMC Genomics 23:809. https://doi.org/10.1186/s12864-022-09040-3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Miller B, Kim SJ, Kumagai H, Mehta HH, Xiang W, Liu J, Yen K, Cohen P (2020) Peptides derived from small mitochondrial open reading frames: genomic, biological, and therapeutic implications. Exp Cell Res 393:112056. https://doi.org/10.1016/j.yexcr.2020.112056

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Kienzle L, Bettinazzi S, Choquette T, Brunet M, Khorami HH, Jacques JF, Moreau M, Roucou X, Landry CR, Angers A, Breton S (2023) A small protein coded within the mitochondrial canonical gene nd4 regulates mitochondrial bioenergetics. BMC Biol 21:111. https://doi.org/10.1186/s12915-023-01609-y

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Andrews S (2010) FastQC: A quality control tool for high throughput sequence Data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

  37. Dierckxsens N, Mardulyn P, Smits G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45:e18. https://doi.org/10.1093/nar/gkw955

    Article  PubMed  CAS  Google Scholar 

  38. Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69:313–319. https://doi.org/10.1016/j.ympev.2012.08.023

    Article  PubMed  Google Scholar 

  39. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Conant GC, Wolfe KH (2008) GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics 24:861–862. https://doi.org/10.1093/bioinformatics/btm598

    Article  PubMed  CAS  Google Scholar 

  41. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. https://doi.org/10.1006/jmbi.2000.4315

    Article  PubMed  CAS  Google Scholar 

  42. Hallgren J, Tsirigos KD, Pedersen MD et al (2022) DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. BioRxiv. https://doi.org/10.1101/2022.04.08.487609

    Article  Google Scholar 

  43. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Gissi C, Iannelli F, Pesole G (2008) Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity (Edinb) 101:301–320. https://doi.org/10.1038/hdy.2008.62

    Article  PubMed  CAS  Google Scholar 

  47. Breton S, Stewart DT, Hoeh WR (2010) Characterization of a mitochondrial ORF from the gender-associated mtDNAs of Mytilus spp. (Bivalvia: Mytilidae): identification of the “missing” ATPase 8 gene. Mar Genomics 3:11–18. https://doi.org/10.1016/j.margen.2010.01.001

    Article  PubMed  Google Scholar 

  48. Smietanka B, Burzyński A, Wenne R (2010) Comparative genomics of marine mussels (Mytilus spp.) gender associated mtDNA: rapidly evolving atp8. J Mol Evol 71:385–400. https://doi.org/10.1007/s00239-010-9393-4

    Article  ADS  PubMed  CAS  Google Scholar 

  49. Egger B, Bachmann L, Fromm B (2017) Atp8 is in the ground pattern of flatworm mitochondrial genomes. BMC Genomics 18:414. https://doi.org/10.1186/s12864-017-3807-2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Zhao B, Gao S, Zhao M, Lv H, Song J, Wang H, Zeng Q, Liu J (2022) Mitochondrial genomic analyses provide new insights into the “missing” atp8 and adaptive evolution of Mytilidae. BMC Genomics 23:738. https://doi.org/10.1186/s12864-022-08940-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Lubośny M, Przyłucka A, Śmietanka B, Breton S, Burzyński A (2018) Actively transcribed and expressed atp8 gene in Mytilus edulis mussels. PeerJ 6:e4897. https://doi.org/10.7717/peerj.4897

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Kim S, Karagozlu MZ, Kim C (2017) Phylogenetic investigations of Lingula anatina among some northwestern Pacific populations, based on mitochondrial DNA cytochrome c oxidase subunit I gene. J Asia-Pacific Biodiversity 10:162–166

    Article  Google Scholar 

  53. Xu W, Jameson D, Tang B, Higgs PG (2006) The relationship between the rate of molecular evolution and the rate of genome rearrangement in animal mitochondrial genomes. J Mol Evol 63:375–392. https://doi.org/10.1007/s00239-005-0246-5

    Article  ADS  PubMed  CAS  Google Scholar 

  54. Goto R, Takano T, Seike K, Yamashita M, Paulay G, Rodgers KS, Hunter CL, Tongkerd P, Sato S, Hong JS, Endo K (2022) Stasis and diversity in living fossils: species delimitation and evolution of lingulid brachiopods. Mol Phylogenet Evol 175:107460. https://doi.org/10.1016/j.ympev.2022.107460

    Article  PubMed  CAS  Google Scholar 

  55. Lomsadze A, Gemayel K, Tang S, Borodovsky M (2018) Modeling leaderless transcription and atypical genes results in more accurate gene prediction in prokaryotes. Genome Res 28:1079–1089. https://doi.org/10.1101/gr.230615.117

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

The author thanks D. Guerra for assistance with lab experiments.

Funding

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) [RGPIN-2019–04076] to S. Br. S. Br. holds the Canada Research Chair (Tier 2) in Mitochondrial Evolutionary Biology.

Author information

Authors and Affiliations

Authors

Contributions

SB contributed to the study conception and design. Specimen collection and identification were performed by staff of Waikiki Aquarium (Hawaii, USA). Data curation, analysis, representation and writing were performed by SB.

Corresponding author

Correspondence to Sophie Breton.

Ethics declarations

Competing interests

The author declares that there are no relevant financial or non-financial interests.

Ethical approval

No specific permission was needed for the collection of L. reevii.

Consent to participate

Not applicable.

Consent to publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 28 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Breton, S. Comparative mitogenomics of Brachiopods reveals conservatism in articulate species and unusualness in inarticulate species. Mol Biol Rep 51, 298 (2024). https://doi.org/10.1007/s11033-024-09270-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11033-024-09270-6

Keywords

Navigation