Skip to main content
SpringerLink
Log in

An exceptional case of mitochondrial tRNA duplication-deletion events in blood-feeding leeches

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

With few exceptions, animal mitochondrial genomes are impressively conserved with regard to gene arrangement (synteny). For certain taxonomic groups, specific genomic “hotspot” regions present high levels of gene rearrangements. This is the case for the region between the mitochondrial genes cox2 and atp8 across Annelida, particularly in members of the blood-feeding leeches of the genus Placobdella, for which duplications and deletions of trnD have been detected. Analyses of the intergenic region between cox2 and atp8 of 21 species of Placobdella broadly collected in Canada, Mexico, Portugal, and the USA revealed numerous instances of trnD duplication restricted to the species of Placobdella, and it can be inferred based on the phylogenetic position of samples with a single trnD copy that the duplicated condition is independently lost on five occasions. In species with the duplicated trnD, great variation in the size of insertions between both copies, in the secondary structure of the trnD products, and in their respective anticodon were found. For each of three species (Placobdella rugosa, P. ringueleti, and P. lamothei), samples collected from different localities exhibit different gene arrangements, revealing an unexpected amount of intraspecific variation. The rate at which rearrangements are occurring in this mitogenome region within Placobdella has no known equivalent in the animal kingdom and we propose it as a hotspot for tRNA genes duplication-deletion. Our findings are partially compatible with a “tandem duplication and random loss” model of evolution, however in species with just one trnD, it is the second copy the one that we inferred is eliminated. This is, to our knowledge, the first study where such changes are mapped in a phylogeny looking to reveal the state of the ancestor of the group.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Sequence data that support the findings of this study have been deposited in GenBank with the accession codes [MK789600-MK789637].

References

  • Arizza, V., Sacco, F., Russo, D., Scardino, R., Arculeo, M., Vamberger, M., & Marrone, F. (2016). The good, the bad and the ugly: Emys trinacris, Placobdella costata and Haemogregarina stepanowi in Sicily (Testudines, Annelida and Apicomplexa). Folia Parasitologica, 63, 1.

    Article  Google Scholar 

  • Bernt, M., Donath, A., Jühling, F., Externbrink, F., Florentz, C., Fritzsch, G., Pütz, J., Middendorf, M., & Stadler, P. F. (2013). MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution, 69(2), 313–319.

    Article  PubMed  Google Scholar 

  • Bielecki, A., Cichocka, J. M., Jabłoński, A., Jeleń, I., Ropelewska, E., Biedunkiewicz, A., et al. (2012). Coexistence of Placobdella costata (Fr. Müller, 1846) (Hirudinida: Glossiphoniidae) and mud turtle Emys orbicularis. Biologia, 67(4), 731–738.

    Article  Google Scholar 

  • Boore, J. L. (1999). Animal mitochondrial genomes. Nucleic Acids Research, 27(8), 1767–1780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boore, J. L. (2000). The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. In J. Nadeau & D. Sankoff (Eds.), Comparative genomics (pp. 133–147). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Boore, J. L., & Brown, W. M. (2000). Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Molecular Biology and Evolution, 17(1), 87–106.

    Article  CAS  PubMed  Google Scholar 

  • Boore, J. L., Collins, T. M., Stanton, D., Daehler, L. L., & Brown, W. M. (1995). Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature, 376, 163–165.

    Article  CAS  PubMed  Google Scholar 

  • Boore, J. L., Macey, J. R., & Medina, M. (2005). Sequencing and comparing whole mitochondrial genomes of animals. Methods in Enzymology, 395, 311–348.

    Article  CAS  PubMed  Google Scholar 

  • de Carle, D., Oceguera-Figueroa, A., Tessler, M., Siddall, M. E., & Kvist, S. (2017). Phylogenetic analysis of Placobdella (Hirudinea: Rhynchobdellida: Glossiphoniidae) with consideration of COI variation. Molecular Phylogenetics and Evolution, 114, 234–248.

    Article  PubMed  CAS  Google Scholar 

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature methods, 9(8), 772–772.

  • Dowton, M., & Austin, A. D. (1999). Evolutionary dynamics of a mitochondrial rearrangement" hot spot" in the Hymenoptera. Molecular Biology and Evolution, 16(2), 298–309.

    Article  CAS  PubMed  Google Scholar 

  • Dowton, M., & Campbell, N. J. (2001). Intramitochondrial recombination–is it why some mitochondrial genes sleep around? Trends in Ecology & Evolution, 16(6), 269–271.

    Article  CAS  Google Scholar 

  • Dowton, M., Cameron, S. L., Dowavic, J. I., Austin, A. D., & Whiting, M. F. (2009). Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Molecular Biology and Evolution, 26(7), 1607–1617.

    Article  CAS  PubMed  Google Scholar 

  • Eberhard, J. R., Wright, T. F., & Bermingham, E. (2001). Duplication and concerted evolution of the mitochondrial control region in the parrot genus Amazona. Molecular Biology and Evolution, 18(7), 1330–1342.

    Article  CAS  PubMed  Google Scholar 

  • Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59(3), 307–321.

  • Jacobs, H. T., Asakawa, S., Araki, T., Miura, K. I., Smith, M. J., & Watanabe, K. (1989). Conserved tRNA gene cluster in starfish mitochondrial DNA. Current Genetics, 15(3), 193–206.

    Article  CAS  PubMed  Google Scholar 

  • Kalendar, R., Lee, D., & Schulman, A. H. (2009). FastPCR software for PCR primer and probe design and repeat search. Genes, Genomes and Genomics, 3(1), 1–14.

    Google Scholar 

  • Katoh, K., Rozewicki, J., & Yamada, K. D. (2019). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20(4), 1160–1166.

  • Kumazawa, Y., & Nishida, M. (1995). Variations in mitochondrial tRNA gene organization of reptiles as phylogenetic markers. Molecular Biology and Evolution, 12(5), 759–772.

    CAS  PubMed  Google Scholar 

  • Lanfear, R., Calcott, B., Ho, S. Y., & Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29(6), 1695–1701.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X., Luo, D., Zhao, Y., Zhang, Q., & Zhang, J. (2017). Complete mithochondrial genome of Ozobranchus jantseanus (Hirudinida: Arhychobdellida: Ozobranchidae). Mitochondrial DNA Part B, 2(1), 232–233.

    Article  PubMed  PubMed Central  Google Scholar 

  • López-Jiménez, S., & Oceguera-Figueroa, A. (2009). New species of rhynchobdellid leech (Hirudinea: Glossiphoniidae): a parasite of turtles from Chiapas, Mexico. Journal of Parasitology, 95(6), 1356–1360.

    Article  Google Scholar 

  • Lowe, T. M., & Chan, P. P. (2016). tRNAscan-SE on-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Research, 44(W1), W54–W57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macey, J. R., Schulte 2nd, J. A., Larson, A., & Papenfuss, T. J. (1998). Tandem duplication via light-strand synthesis may provide a precursor for mitochondrial genomic rearrangement. Molecular Biology and Evolution, 15(1), 71–75.

    Article  CAS  PubMed  Google Scholar 

  • Mack, J., de Carle, D., & Kvist, S. (2019). Prey, populations, and the Pleistocene: evidence for low COI variation in a widespread North American leech. Mitochondrial DNA Part A, 30(6), 749–763.

    Article  CAS  Google Scholar 

  • Maddison, W. P. (2008). Mesquite: a modular system for evolutionary analysis. Evolution, 62, 1103–1118.

    Article  Google Scholar 

  • Miya, M., Kawaguchi, A., & Nishida, M. (2001). Mitogenomic exploration of higher teleostean phylogenies: a case study for moderate-scale evolutionary genomics with 38 newly determined complete mitochondrial DNA sequences. Molecular Biology and Evolution, 18(11), 1993–2009.

    Article  CAS  PubMed  Google Scholar 

  • Moser, W. E., Bowerman, J., Hovingh, P., Pearl, C. A., & Oceguera-Figueroa, A. (2014a). New host and distribution records of the leech Placobdella sophieae Oceguera-Figueroa et al., 2010 (Hirudinida: Glossiphoniidae). Comparative Parasitology, 81(2), 199–203.

    Article  Google Scholar 

  • Moser, W. E., Richardson, D. J., Hammond, C. I., & Lazo-Wasem, E. A. (2014b). Redescription and molecular characterization of Placobdella hollensis (Whitman, 1892)(Hirudinida: Glossiphoniidae). Bulletin of the Peabody Museum of Natural History, 55(1), 49–54.

    Article  Google Scholar 

  • Moser, W. E., Richardson, D. J., & Lazo-Wasem, E. A. (2016). Distribution of Placobdella ornata (Verrill, 1872) (Hirudinida: Glossiphoniidae). Bulletin of the Peabody Museum of Natural History, 57(2), 175-179.

  • Mueller, R. L., & Boore, J. L. (2005). Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders. Molecular Biology and Evolution, 22(10), 2104–2112.

    Article  CAS  PubMed  Google Scholar 

  • Nikitina, A., Babenko, V., Akopian, T., Shirokov, D., Manuvera, V., Kurdyumov, A., et al. (2016). Draft mitochondrial genomes of Hirudo medicinalis and Hirudo verbana (Annelida, Hirudinea). Mitochondrial DNA Part B, 1(1), 254–256.

    Article  PubMed  PubMed Central  Google Scholar 

  • Oceguera-Figueroa, A., & Pacheco-Chaves, B. (2012). Registros de sanguijuelas de Costa Rica y clave para la identificación de las especies con redescripción de Cylicobdella costaricae. Revista Mexicana de Biodiversidad, 83(4), 946–957.

    Google Scholar 

  • Oceguera-Figueroa, A., & Siddall, M. E. (2008). Placobdella lamothei n. sp. (Hirudinea: Glossiphoniidae), a new leech parasite of freshwater turtles from Estado de México, Mexico. Revista Mexicana de Biodiversidad, 79, 135S–139S.

    Article  Google Scholar 

  • Oceguera-Figueroa, A., Kvist, S., Watson, S. C., Sankar, D. F., Overstreet, R. M., & Siddall, M. E. (2010). Leech collections from Washington state, with the description of two new species of Placobdella (Annelida: Glossiphoniidae). American Museum Novitates, 2010(3701), 1–15.

    Article  Google Scholar 

  • Oceguera-Figueroa, A., Manzano-Marin, A., Kvist, S., Moya, A., Siddall, M. E., & Latorre, A. (2016). Comparative mitogenomics of leeches (Annelida: Clitellata): Genome conservation and Placobdella-specific trnD gene duplication. PLoS One, 11(5), e0155441.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • San Mauro, D., Gower, D. J., Zardoya, R., & Wilkinson, M. (2005). A hotspot of gene order rearrangement by tandem duplication and random loss in the vertebrate mitochondrial genome. Molecular Biology and Evolution, 23(1), 227–234.

    Article  PubMed  CAS  Google Scholar 

  • Sawyer RT. 1986. Leech biology and behaviour: Feeding biology, ecology, and systematics. Oxford University Press.

  • Siddall, M. E., & Gaffney, E. S. (2004). Observations on the leech Placobdella ornata feeding from bony tissues of turtles. Journal of Parasitology, 90(5), 1186–1189.

    Article  Google Scholar 

  • Siddall, M. E., Budinoff, R. B., & Borda, E. (2005). Phylogenetic evaluation of systematics and biogeography of the leech family Glossiphoniidae. Invertebrate Systematics, 19(2), 105–112.

    Article  Google Scholar 

  • Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tessler, M., de Carle, D., Voiklis, M. L., Gresham, O. A., Neumann, J. S., Cios, S., & Siddall, M. E. (2018). Worms that suck: phylogenetic analysis of Hirudinea solidifies the position of Acanthobdellida and necessitates the dissolution of Rhynchobdellida. Molecular Phylogenetics and Evolution, 127, 129–134.

    Article  PubMed  Google Scholar 

  • Wang, Y., Huang, M., Wang, R., & Fu, L. (2018). Complete mitochondrial genome of the fish leech Zeylanicobdella arugamensis. Mitochondrial DNA Part B, 3(2), 659–660.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu, Y., Nie, J., Hou, J., Xiao, L., & Lv, P. (2016). Complete mitochondrial genome of Hirudo nipponia (Annelida, Hirudinea). Mitochondrial DNA Part A, 27(1), 257–258.

    Article  CAS  Google Scholar 

  • Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., & Madden, T. L. (2012). Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics, 13(1), 134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Andrea Jiménez Marín, Ofelia Delgado Hernández, Laura Márquez Valdelamar, Nelly López Ortíz, Oliver Haddrath, and Kristen Choffe assisted in the generation of DNA sequences.

Funding

This project was funded by the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica IN210318 (PAPIIT-UNAM) and Consejo Nacional de Ciencia y Tecnología (CONACYT) Ciencia Básica 220408 to AO-F. CONACYT provided a scholarship to JJ-A. UNAM’s Programa de Apoyo a los Estudios de Posgrado provided founding for an internship in the Royal Ontario Museum, where funding was supported by an NSERC Discovery Grant to SK. Mark Siddall kindly provided several DNA samples of Placobdella species that were used in this study.

Author information

Authors and Affiliations

  1. Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, Coyoacán, C.P. 04510, Ciudad de México, Mexico

    J. Jiménez-Armenta

  2. Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de Mexico, Tercer circuito s/n, Ciudad Universitaria, Copilco, C.P. 04510, Coyoacán, Cuidad de Mexico, Mexico

    J. Jiménez-Armenta & A. Oceguera-Figueroa

  3. Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario, M5S 2B4, Canada

    S. Kvist

  4. Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario, M5S 2C6, Canada

    S. Kvist

Authors
  1. J. Jiménez-Armenta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Kvist
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Oceguera-Figueroa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Oceguera-Figueroa.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiménez-Armenta, J., Kvist, S. & Oceguera-Figueroa, A. An exceptional case of mitochondrial tRNA duplication-deletion events in blood-feeding leeches. Org Divers Evol 20, 221–231 (2020). https://doi.org/10.1007/s13127-020-00431-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-020-00431-6

Keywords

Search

Navigation