Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer

Andrea Strakova, Thomas J. Nicholls, Adrian Baez-Ortega, Máire Ní Leathlobhair, Alexander T. Sampson, Katherine Hughes, Isobelle A.G. Bolton, Kevin Gori, Jinhong Wang, Ilona Airikkala-Otter, Janice L. Allen, Karen M. Allum, Clara L. Arnold, Leontine Bansse-Issa, Thinlay N. Bhutia, Jocelyn L. Bisson, Kelli Blank, Cristóbal Briceño, Artemio Castillo Domracheva, Anne M. CorriganHugh R. Cran, Jane T. Crawford, Stephen M. Cutter, Eric Davis, Karina F. de Castro, Andrigo B. De Nardi, Anna P. de Vos, Laura Delgadillo Keenan, Edward M. Donelan, Adela R. Espinoza Huerta, Ibikunle A. Faramade, Mohammed Fazil, Eleni Fotopoulou, Skye N. Fruean, Fanny Gallardo-Arrieta, Olga Glebova, Pagona G. Gouletsou, Rodrigo F. Häfelin Manrique, Joaquim J.G.P. Henriques, Rodrigo S. Horta, Natalia Ignatenko, Yaghouba Kane, Cathy King, Debbie Koenig, Ada Krupa, Steven J. Kruzeniski, Marta Lanza-Perea, Mihran Lazyan, Adriana M. Lopez Quintana, Thibault Losfelt, Gabriele Marino, Simón Martínez Castañeda, Mayra F. Martínez-López, Bedan M. Masuruli, Michael Meyer, Edward J. Migneco, Berna Nakanwagi, Karter B. Neal, Winifred Neunzig, Sally J. Nixon, Antonio Ortega-Pacheco, Francisco Pedraza-Ordoñez, Maria C. Peleteiro, Katherine Polak, Ruth J. Pye, Juan C. Ramirez-Ante, John F. Reece, Jose Rojas Gutierrez, Haleema Sadia, Sheila K. Schmeling, Olga Shamanova, Alan G. Sherlock, Audrey E. Steenland-Smit, Alla Svitich, Lester J. Tapia Martínez, Ismail Thoya Ngoka, Cristian G. Torres, Elizabeth M. Tudor, Mirjam G. van der Wel, Bogdan A. Vițălaru, Sevil A. Vural, Oliver Walkinton, Alvaro S. Wehrle-Martinez, Sophie A.E. Widdowson, Irina Zvarich, Patrick F. Chinnery, Maria Falkenberg, Claes M. Gustafsson, Elizabeth P. Murchison

Research output: Contribution to journalArticle

Abstract

Autonomous replication and segregation of mitochondrial DNA (mtDNA) creates the potential for evolutionary conflict driven by emergence of haplotypes under positive selection for ‘selfish’ traits, such as replicative advantage. However, few cases of this phenomenon arising within natural populations have been described. Here, we survey the frequency of mtDNA horizontal transfer within the canine transmissible venereal tumour (CTVT), a contagious cancer clone that occasionally acquires mtDNA from its hosts. Remarkably, one canine mtDNA haplotype, A1d1a, has repeatedly and recently colonised CTVT cells, recurrently replacing incumbent CTVT haplotypes. An A1d1a control region polymorphism predicted to influence transcription is fixed in the products of an A1d1a recombination event and occurs somatically on other CTVT mtDNA backgrounds. We present a model whereby ‘selfish’ positive selection acting on a regulatory variant drives repeated fixation of A1d1a within CTVT cells.

Original languageEnglish (US)
Article number3059
JournalNature communications
Volume11
Issue number1
DOIs
StatePublished - Dec 1 2020

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

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    Strakova, A., Nicholls, T. J., Baez-Ortega, A., Ní Leathlobhair, M., Sampson, A. T., Hughes, K., Bolton, I. A. G., Gori, K., Wang, J., Airikkala-Otter, I., Allen, J. L., Allum, K. M., Arnold, C. L., Bansse-Issa, L., Bhutia, T. N., Bisson, J. L., Blank, K., Briceño, C., Castillo Domracheva, A., ... Murchison, E. P. (2020). Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer. Nature communications, 11(1), [3059]. https://doi.org/10.1038/s41467-020-16765-w