Complete vertebrate mitogenomes reveal widespread repeats and gene duplications

doi:10.1186/s13059-021-02336-9

Complete vertebrate mitogenomes reveal widespread repeats and gene duplications

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26 Scopus citations

Abstract

Background: Modern sequencing technologies should make the assembly of the relatively small mitochondrial genomes an easy undertaking. However, few tools exist that address mitochondrial assembly directly. Results: As part of the Vertebrate Genomes Project (VGP) we develop mitoVGP, a fully automated pipeline for similarity-based identification of mitochondrial reads and de novo assembly of mitochondrial genomes that incorporates both long (> 10 kbp, PacBio or Nanopore) and short (100–300 bp, Illumina) reads. Our pipeline leads to successful complete mitogenome assemblies of 100 vertebrate species of the VGP. We observe that tissue type and library size selection have considerable impact on mitogenome sequencing and assembly. Comparing our assemblies to purportedly complete reference mitogenomes based on short-read sequencing, we identify errors, missing sequences, and incomplete genes in those references, particularly in repetitive regions. Our assemblies also identify novel gene region duplications. The presence of repeats and duplications in over half of the species herein assembled indicates that their occurrence is a principle of mitochondrial structure rather than an exception, shedding new light on mitochondrial genome evolution and organization. Conclusions: Our results indicate that even in the “simple” case of vertebrate mitogenomes the completeness of many currently available reference sequences can be further improved, and caution should be exercised before claiming the complete assembly of a mitogenome, particularly from short reads alone.

Original language	English
Article number	120
Journal	Genome Biology
Volume	22
Issue number	1
DOIs	https://doi.org/10.1186/s13059-021-02336-9
State	Published - Dec 2021

Bibliographical note

Funding Information:
We thank the contributors of the VGP on the first 125 species for letting us use data for generating mitochondrial genome assemblies; in particular, they are Alexander N. G. Kirschel, Andrew Digby, Andrew Veale, Anne Bronikowski, Bob Murphy, Bruce Robertson, Clare Baker, Camila Mazzoni, Christopher Balakrishnan, Chul Lee, Daniel Mead, Emma Teeling, Erez Lieberman Aiden, Erica Todd, Evan Eichler, Gavin J.P. Naylor, Guojie Zhang, Jeramiah Smith, Jochen Wolf, Justin Touchon, Kira Delmore, Kjetill Jakobsen, Lisa Komoroske, Mark Wilkinson, Martin Genner, Martin Pšenička, Matthew Fuxjager, Mike Stratton, Miriam Liedvogel, Neil Gemmell, Piotr Minias, Peter O. Dunn, Peter Sudmant, Phil Morin, Sadequr Rahman, Qasim Ayub, Robert Kraus, Sonja Vernes, Steve Smith, Tanya Lama, Taylor Edwards, Tim Smith, Tom Gilbert, Tomas Marques-Bonet, Tony Einfeldt, Byrappa Venkatesh, Warren Johnson, Wes Warren, and Yury Bukhman. We are grateful to the Ngā Papatipu Rūnanga o Murihiku and the Ngāi Tahu for their support in generating the kakapo datasets. We also thank Aureliano Bombarely for his support in testing Organelle_PBA on VGP datasets. The review history is available as Additional file 12. Barbara Cheifet was the primary editor of this article and managed its editorial process and peer review in collaboration with the rest of the editorial team.

Funding Information:
A. R., S. K., and A. M. P. were supported by the Intramural Research Program of the National Human Genome Research Institute, National Institutes of Health. A. R. was also supported by the Korea Health Technology R&D Project through KHIDI, funded by the Ministry of Health & Welfare, Republic of Korea (HI17C2098). F. O. A. was supported by Al-Gannas Qatari Society and The Cultural Village Foundation-Katara, Doha, State of Qatar and Monash University Malaysia. G. F. and E. D. J were supported by Rockefeller University start-up funds and the Howard Hughes Medical Institute. A.A. and M.R.C. received support from the Fondazione Cariplo project no. 2018–2045 and the Italian Ministry of Education, University and Research (MIUR) for Progetti PRIN2017 20174BTC4R and Dipartimenti di Eccellenza Program (2018–2022). R. D. and S. M. received funding from Wellcome grant WT207492.

Publisher Copyright:
© 2021, The Author(s).

Keywords

Assembly
Duplications
Long reads
Mitochondrial DNA
Repeats
Sequencing
Vertebrate

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics
Cell Biology

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10.1186/s13059-021-02336-9

Cite this

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title = "Complete vertebrate mitogenomes reveal widespread repeats and gene duplications",

abstract = "Background: Modern sequencing technologies should make the assembly of the relatively small mitochondrial genomes an easy undertaking. However, few tools exist that address mitochondrial assembly directly. Results: As part of the Vertebrate Genomes Project (VGP) we develop mitoVGP, a fully automated pipeline for similarity-based identification of mitochondrial reads and de novo assembly of mitochondrial genomes that incorporates both long (> 10 kbp, PacBio or Nanopore) and short (100–300 bp, Illumina) reads. Our pipeline leads to successful complete mitogenome assemblies of 100 vertebrate species of the VGP. We observe that tissue type and library size selection have considerable impact on mitogenome sequencing and assembly. Comparing our assemblies to purportedly complete reference mitogenomes based on short-read sequencing, we identify errors, missing sequences, and incomplete genes in those references, particularly in repetitive regions. Our assemblies also identify novel gene region duplications. The presence of repeats and duplications in over half of the species herein assembled indicates that their occurrence is a principle of mitochondrial structure rather than an exception, shedding new light on mitochondrial genome evolution and organization. Conclusions: Our results indicate that even in the “simple” case of vertebrate mitogenomes the completeness of many currently available reference sequences can be further improved, and caution should be exercised before claiming the complete assembly of a mitogenome, particularly from short reads alone.",

keywords = "Assembly, Duplications, Long reads, Mitochondrial DNA, Repeats, Sequencing, Vertebrate",

author = "Giulio Formenti and Arang Rhie and Jennifer Balacco and Bettina Haase and Jacquelyn Mountcastle and Olivier Fedrigo and Samara Brown and Capodiferro, {Marco Rosario} and Al-Ajli, {Farooq O.} and Roberto Ambrosini and Peter Houde and Sergey Koren and Karen Oliver and Michelle Smith and Jason Skelton and Emma Betteridge and Jale Dolucan and Craig Corton and Iliana Bista and James Torrance and Alan Tracey and Jonathan Wood and Marcela Uliano-Silva and Kerstin Howe and Shane McCarthy and Sylke Winkler and Woori Kwak and Jonas Korlach and Arkarachai Fungtammasan and Daniel Fordham and Vania Costa and Simon Mayes and Matteo Chiara and Horner, {David S.} and Eugene Myers and Richard Durbin and Alessandro Achilli and Braun, {Edward L.} and Phillippy, {Adam M.} and Jarvis, {Erich D.} and Kirschel, {Alexander N.G.} and Andrew Digby and Andrew Veale and Anne Bronikowski and Bob Murphy and Bruce Robertson and Clare Baker and Camila Mazzoni and Christopher Balakrishnan and Jeramiah Smith",

note = "Funding Information: We thank the contributors of the VGP on the first 125 species for letting us use data for generating mitochondrial genome assemblies; in particular, they are Alexander N. G. Kirschel, Andrew Digby, Andrew Veale, Anne Bronikowski, Bob Murphy, Bruce Robertson, Clare Baker, Camila Mazzoni, Christopher Balakrishnan, Chul Lee, Daniel Mead, Emma Teeling, Erez Lieberman Aiden, Erica Todd, Evan Eichler, Gavin J.P. Naylor, Guojie Zhang, Jeramiah Smith, Jochen Wolf, Justin Touchon, Kira Delmore, Kjetill Jakobsen, Lisa Komoroske, Mark Wilkinson, Martin Genner, Martin P{\v s}eni{\v c}ka, Matthew Fuxjager, Mike Stratton, Miriam Liedvogel, Neil Gemmell, Piotr Minias, Peter O. Dunn, Peter Sudmant, Phil Morin, Sadequr Rahman, Qasim Ayub, Robert Kraus, Sonja Vernes, Steve Smith, Tanya Lama, Taylor Edwards, Tim Smith, Tom Gilbert, Tomas Marques-Bonet, Tony Einfeldt, Byrappa Venkatesh, Warren Johnson, Wes Warren, and Yury Bukhman. We are grateful to the Ngā Papatipu Rūnanga o Murihiku and the Ngāi Tahu for their support in generating the kakapo datasets. We also thank Aureliano Bombarely for his support in testing Organelle_PBA on VGP datasets. The review history is available as Additional file 12. Barbara Cheifet was the primary editor of this article and managed its editorial process and peer review in collaboration with the rest of the editorial team. Funding Information: A. R., S. K., and A. M. P. were supported by the Intramural Research Program of the National Human Genome Research Institute, National Institutes of Health. A. R. was also supported by the Korea Health Technology R&D Project through KHIDI, funded by the Ministry of Health & Welfare, Republic of Korea (HI17C2098). F. O. A. was supported by Al-Gannas Qatari Society and The Cultural Village Foundation-Katara, Doha, State of Qatar and Monash University Malaysia. G. F. and E. D. J were supported by Rockefeller University start-up funds and the Howard Hughes Medical Institute. A.A. and M.R.C. received support from the Fondazione Cariplo project no. 2018–2045 and the Italian Ministry of Education, University and Research (MIUR) for Progetti PRIN2017 20174BTC4R and Dipartimenti di Eccellenza Program (2018–2022). R. D. and S. M. received funding from Wellcome grant WT207492. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

doi = "10.1186/s13059-021-02336-9",

language = "English",

volume = "22",

number = "1",

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TY - JOUR

T1 - Complete vertebrate mitogenomes reveal widespread repeats and gene duplications

AU - Formenti, Giulio

AU - Rhie, Arang

AU - Balacco, Jennifer

AU - Haase, Bettina

AU - Mountcastle, Jacquelyn

AU - Fedrigo, Olivier

AU - Brown, Samara

AU - Capodiferro, Marco Rosario

AU - Al-Ajli, Farooq O.

AU - Ambrosini, Roberto

AU - Houde, Peter

AU - Koren, Sergey

AU - Oliver, Karen

AU - Smith, Michelle

AU - Skelton, Jason

AU - Betteridge, Emma

AU - Dolucan, Jale

AU - Corton, Craig

AU - Bista, Iliana

AU - Torrance, James

AU - Tracey, Alan

AU - Wood, Jonathan

AU - Uliano-Silva, Marcela

AU - Howe, Kerstin

AU - McCarthy, Shane

AU - Winkler, Sylke

AU - Kwak, Woori

AU - Korlach, Jonas

AU - Fungtammasan, Arkarachai

AU - Fordham, Daniel

AU - Costa, Vania

AU - Mayes, Simon

AU - Chiara, Matteo

AU - Horner, David S.

AU - Myers, Eugene

AU - Durbin, Richard

AU - Achilli, Alessandro

AU - Braun, Edward L.

AU - Phillippy, Adam M.

AU - Jarvis, Erich D.

AU - Kirschel, Alexander N.G.

AU - Digby, Andrew

AU - Veale, Andrew

AU - Bronikowski, Anne

AU - Murphy, Bob

AU - Robertson, Bruce

AU - Baker, Clare

AU - Mazzoni, Camila

AU - Balakrishnan, Christopher

AU - Smith, Jeramiah

N1 - Funding Information: We thank the contributors of the VGP on the first 125 species for letting us use data for generating mitochondrial genome assemblies; in particular, they are Alexander N. G. Kirschel, Andrew Digby, Andrew Veale, Anne Bronikowski, Bob Murphy, Bruce Robertson, Clare Baker, Camila Mazzoni, Christopher Balakrishnan, Chul Lee, Daniel Mead, Emma Teeling, Erez Lieberman Aiden, Erica Todd, Evan Eichler, Gavin J.P. Naylor, Guojie Zhang, Jeramiah Smith, Jochen Wolf, Justin Touchon, Kira Delmore, Kjetill Jakobsen, Lisa Komoroske, Mark Wilkinson, Martin Genner, Martin Pšenička, Matthew Fuxjager, Mike Stratton, Miriam Liedvogel, Neil Gemmell, Piotr Minias, Peter O. Dunn, Peter Sudmant, Phil Morin, Sadequr Rahman, Qasim Ayub, Robert Kraus, Sonja Vernes, Steve Smith, Tanya Lama, Taylor Edwards, Tim Smith, Tom Gilbert, Tomas Marques-Bonet, Tony Einfeldt, Byrappa Venkatesh, Warren Johnson, Wes Warren, and Yury Bukhman. We are grateful to the Ngā Papatipu Rūnanga o Murihiku and the Ngāi Tahu for their support in generating the kakapo datasets. We also thank Aureliano Bombarely for his support in testing Organelle_PBA on VGP datasets. The review history is available as Additional file 12. Barbara Cheifet was the primary editor of this article and managed its editorial process and peer review in collaboration with the rest of the editorial team. Funding Information: A. R., S. K., and A. M. P. were supported by the Intramural Research Program of the National Human Genome Research Institute, National Institutes of Health. A. R. was also supported by the Korea Health Technology R&D Project through KHIDI, funded by the Ministry of Health & Welfare, Republic of Korea (HI17C2098). F. O. A. was supported by Al-Gannas Qatari Society and The Cultural Village Foundation-Katara, Doha, State of Qatar and Monash University Malaysia. G. F. and E. D. J were supported by Rockefeller University start-up funds and the Howard Hughes Medical Institute. A.A. and M.R.C. received support from the Fondazione Cariplo project no. 2018–2045 and the Italian Ministry of Education, University and Research (MIUR) for Progetti PRIN2017 20174BTC4R and Dipartimenti di Eccellenza Program (2018–2022). R. D. and S. M. received funding from Wellcome grant WT207492. Publisher Copyright: © 2021, The Author(s).

PY - 2021/12

Y1 - 2021/12

N2 - Background: Modern sequencing technologies should make the assembly of the relatively small mitochondrial genomes an easy undertaking. However, few tools exist that address mitochondrial assembly directly. Results: As part of the Vertebrate Genomes Project (VGP) we develop mitoVGP, a fully automated pipeline for similarity-based identification of mitochondrial reads and de novo assembly of mitochondrial genomes that incorporates both long (> 10 kbp, PacBio or Nanopore) and short (100–300 bp, Illumina) reads. Our pipeline leads to successful complete mitogenome assemblies of 100 vertebrate species of the VGP. We observe that tissue type and library size selection have considerable impact on mitogenome sequencing and assembly. Comparing our assemblies to purportedly complete reference mitogenomes based on short-read sequencing, we identify errors, missing sequences, and incomplete genes in those references, particularly in repetitive regions. Our assemblies also identify novel gene region duplications. The presence of repeats and duplications in over half of the species herein assembled indicates that their occurrence is a principle of mitochondrial structure rather than an exception, shedding new light on mitochondrial genome evolution and organization. Conclusions: Our results indicate that even in the “simple” case of vertebrate mitogenomes the completeness of many currently available reference sequences can be further improved, and caution should be exercised before claiming the complete assembly of a mitogenome, particularly from short reads alone.

AB - Background: Modern sequencing technologies should make the assembly of the relatively small mitochondrial genomes an easy undertaking. However, few tools exist that address mitochondrial assembly directly. Results: As part of the Vertebrate Genomes Project (VGP) we develop mitoVGP, a fully automated pipeline for similarity-based identification of mitochondrial reads and de novo assembly of mitochondrial genomes that incorporates both long (> 10 kbp, PacBio or Nanopore) and short (100–300 bp, Illumina) reads. Our pipeline leads to successful complete mitogenome assemblies of 100 vertebrate species of the VGP. We observe that tissue type and library size selection have considerable impact on mitogenome sequencing and assembly. Comparing our assemblies to purportedly complete reference mitogenomes based on short-read sequencing, we identify errors, missing sequences, and incomplete genes in those references, particularly in repetitive regions. Our assemblies also identify novel gene region duplications. The presence of repeats and duplications in over half of the species herein assembled indicates that their occurrence is a principle of mitochondrial structure rather than an exception, shedding new light on mitochondrial genome evolution and organization. Conclusions: Our results indicate that even in the “simple” case of vertebrate mitogenomes the completeness of many currently available reference sequences can be further improved, and caution should be exercised before claiming the complete assembly of a mitogenome, particularly from short reads alone.

KW - Assembly

KW - Duplications

KW - Long reads

KW - Mitochondrial DNA

KW - Repeats

KW - Sequencing

KW - Vertebrate

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U2 - 10.1186/s13059-021-02336-9

DO - 10.1186/s13059-021-02336-9

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M1 - 120

ER -

Complete vertebrate mitogenomes reveal widespread repeats and gene duplications

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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