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

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.

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Data availability

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

References

  1. 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.

  2. 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.

  3. 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.

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

  5. 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.

  6. 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.

  7. 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.

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

  9. 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.

  10. 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.

  11. 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.

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

  13. 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.

  14. 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.

  15. 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.

  16. 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.

  17. 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.

  18. 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.

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

  20. 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.

  21. 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.

  22. 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.

  23. 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.

  24. 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.

  25. 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.

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

  27. 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.

  28. 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.

  29. 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.

  30. 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.

  31. 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.

  32. 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.

  33. 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.

  34. 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.

  35. 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.

  36. 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.

  37. 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.

  38. 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.

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

  40. 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.

  41. 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.

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

  43. 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.

  44. 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.

  45. 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.

  46. 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.

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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.

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Correspondence to A. Oceguera-Figueroa.

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

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Keywords

  • tRNA duplication
  • tRNA deletion
  • Mitochondrial evolution
  • Placobdella