Genome sequencing and transcriptomic analysis of the Andean killifish Orestias ascotanensis reveals adaptation to high-altitude aquatic life

Alex Di Genova; Gino Nardocci; Rodrigo Maldonado-Agurto; Christian Hodar; Camilo Valdivieso; Pamela Morales; Felipe Gajardo; Raquel Marina; Rodrigo A. Gutiérrez; Ariel Orellana; Veronica Cambiazo; Mauricio González; Alvaro Glavic; Marco A. Mendez; Alejandro Maass; Miguel L. Allende; Martin A. Montecino

doi:10.1016/j.ygeno.2021.12.018

Genome sequencing and transcriptomic analysis of the Andean killifish Orestias ascotanensis reveals adaptation to high-altitude aquatic life

Alex Di Genova, Gino Nardocci, Rodrigo Maldonado-Agurto, Christian Hodar, Camilo Valdivieso, Pamela Morales, Felipe Gajardo, Raquel Marina, Rodrigo A. Gutiérrez, Ariel Orellana, Veronica Cambiazo, Mauricio González, Alvaro Glavic, Marco A. Mendez, Alejandro Maass, Miguel L. Allende, Martin A. Montecino^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Orestias ascotanensis (Cyprinodontidae) is a teleost pupfish endemic to springs feeding into the Ascotan saltpan in the Chilean Altiplano (3,700 m.a.s.l.) and represents an opportunity to study adaptations to high-altitude aquatic environments. We have de novo assembled the genome of O. ascotanensis at high coverage. Comparative analysis of the O. ascotanensis genome showed an overall process of contraction, including loss of genes related to G-protein signaling, chemotaxis and signal transduction, while there was expansion of gene families associated with microtubule-based movement and protein ubiquitination. We identified 818 genes under positive selection, many of which are involved in DNA repair. Additionally, we identified novel and conserved microRNAs expressed in O. ascotanensis and its closely-related species, Orestias gloriae. Our analysis suggests that positive selection and expansion of genes that preserve genome stability are a potential adaptive mechanism to cope with the increased solar UV radiation to which high-altitude animals are exposed to.

Original language	English
Pages (from-to)	305-315
Number of pages	11
Journal	Genomics
Volume	114
Issue number	1
DOIs	https://doi.org/10.1016/j.ygeno.2021.12.018
State	Published - Jan 2022
Externally published	Yes

Bibliographical note

Funding Information:
This work is part of the Chilean 1000 Genomes Initiative and is carried out within the framework of the Earth Biogenome Project ( www.earthbiogenome.org ). Funding has been provided by ANID/FONDAP 15090007 and 15200002, ANID/FONDECYT 1180606 (to MLA), ANID/FONDECYT 3190720 (to RMA) and ANID/FONDECYT 1200419 (to M Mendez). This research was partially supported by the supercomputing infrastructure of the NLHPC (ECM-02) and ANID-PIA AFB 170001.

Funding Information:
The authors thank Dr. Juan C. Opazo for his technical support with the Phylogenetic Analysis by Maximum Likelihood (PAML) analysis. This work is part of the Chilean 1000 Genomes Initiative and is carried out within the framework of the Earth Biogenome Project (www.earthbiogenome.org). Funding has been provided by ANID/FONDAP 15090007 and 15200002, ANID/FONDECYT 1180606 (to MLA), ANID/FONDECYT 3190720 (to RMA) and ANID/FONDECYT 1200419 (to M Mendez). This research was partially supported by the supercomputing infrastructure of the NLHPC (ECM-02) and ANID-PIA AFB 170001.

Publisher Copyright:
© 2021

Keywords

Altiplano
Desert pupfish
DNA repair
High-altitude
microRNAs
Orestias ascotanensis

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10.1016/j.ygeno.2021.12.018

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Di Genova, A., Nardocci, G., Maldonado-Agurto, R., Hodar, C., Valdivieso, C., Morales, P., Gajardo, F., Marina, R., Gutiérrez, R. A., Orellana, A., Cambiazo, V., González, M., Glavic, A., Mendez, M. A., Maass, A., Allende, M. L., & Montecino, M. A. (2022). Genome sequencing and transcriptomic analysis of the Andean killifish Orestias ascotanensis reveals adaptation to high-altitude aquatic life. Genomics, 114(1), 305-315. https://doi.org/10.1016/j.ygeno.2021.12.018

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title = "Genome sequencing and transcriptomic analysis of the Andean killifish Orestias ascotanensis reveals adaptation to high-altitude aquatic life",

abstract = "Orestias ascotanensis (Cyprinodontidae) is a teleost pupfish endemic to springs feeding into the Ascotan saltpan in the Chilean Altiplano (3,700 m.a.s.l.) and represents an opportunity to study adaptations to high-altitude aquatic environments. We have de novo assembled the genome of O. ascotanensis at high coverage. Comparative analysis of the O. ascotanensis genome showed an overall process of contraction, including loss of genes related to G-protein signaling, chemotaxis and signal transduction, while there was expansion of gene families associated with microtubule-based movement and protein ubiquitination. We identified 818 genes under positive selection, many of which are involved in DNA repair. Additionally, we identified novel and conserved microRNAs expressed in O. ascotanensis and its closely-related species, Orestias gloriae. Our analysis suggests that positive selection and expansion of genes that preserve genome stability are a potential adaptive mechanism to cope with the increased solar UV radiation to which high-altitude animals are exposed to.",

keywords = "Altiplano, Desert pupfish, DNA repair, High-altitude, microRNAs, Orestias ascotanensis",

author = "{Di Genova}, Alex and Gino Nardocci and Rodrigo Maldonado-Agurto and Christian Hodar and Camilo Valdivieso and Pamela Morales and Felipe Gajardo and Raquel Marina and Guti{\'e}rrez, {Rodrigo A.} and Ariel Orellana and Veronica Cambiazo and Mauricio Gonz{\'a}lez and Alvaro Glavic and Mendez, {Marco A.} and Alejandro Maass and Allende, {Miguel L.} and Montecino, {Martin A.}",

note = "Funding Information: This work is part of the Chilean 1000 Genomes Initiative and is carried out within the framework of the Earth Biogenome Project ( www.earthbiogenome.org ). Funding has been provided by ANID/FONDAP 15090007 and 15200002, ANID/FONDECYT 1180606 (to MLA), ANID/FONDECYT 3190720 (to RMA) and ANID/FONDECYT 1200419 (to M Mendez). This research was partially supported by the supercomputing infrastructure of the NLHPC (ECM-02) and ANID-PIA AFB 170001. Funding Information: The authors thank Dr. Juan C. Opazo for his technical support with the Phylogenetic Analysis by Maximum Likelihood (PAML) analysis. This work is part of the Chilean 1000 Genomes Initiative and is carried out within the framework of the Earth Biogenome Project (www.earthbiogenome.org). Funding has been provided by ANID/FONDAP 15090007 and 15200002, ANID/FONDECYT 1180606 (to MLA), ANID/FONDECYT 3190720 (to RMA) and ANID/FONDECYT 1200419 (to M Mendez). This research was partially supported by the supercomputing infrastructure of the NLHPC (ECM-02) and ANID-PIA AFB 170001. Publisher Copyright: {\textcopyright} 2021",

year = "2022",

month = jan,

doi = "10.1016/j.ygeno.2021.12.018",

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Di Genova, A, Nardocci, G, Maldonado-Agurto, R, Hodar, C, Valdivieso, C, Morales, P, Gajardo, F, Marina, R, Gutiérrez, RA, Orellana, A, Cambiazo, V, González, M, Glavic, A, Mendez, MA, Maass, A, Allende, ML & Montecino, MA 2022, 'Genome sequencing and transcriptomic analysis of the Andean killifish Orestias ascotanensis reveals adaptation to high-altitude aquatic life', Genomics, vol. 114, no. 1, pp. 305-315. https://doi.org/10.1016/j.ygeno.2021.12.018

TY - JOUR

T1 - Genome sequencing and transcriptomic analysis of the Andean killifish Orestias ascotanensis reveals adaptation to high-altitude aquatic life

AU - Di Genova, Alex

AU - Nardocci, Gino

AU - Maldonado-Agurto, Rodrigo

AU - Hodar, Christian

AU - Valdivieso, Camilo

AU - Morales, Pamela

AU - Gajardo, Felipe

AU - Marina, Raquel

AU - Gutiérrez, Rodrigo A.

AU - Orellana, Ariel

AU - Cambiazo, Veronica

AU - González, Mauricio

AU - Glavic, Alvaro

AU - Mendez, Marco A.

AU - Maass, Alejandro

AU - Allende, Miguel L.

AU - Montecino, Martin A.

N1 - Funding Information: This work is part of the Chilean 1000 Genomes Initiative and is carried out within the framework of the Earth Biogenome Project ( www.earthbiogenome.org ). Funding has been provided by ANID/FONDAP 15090007 and 15200002, ANID/FONDECYT 1180606 (to MLA), ANID/FONDECYT 3190720 (to RMA) and ANID/FONDECYT 1200419 (to M Mendez). This research was partially supported by the supercomputing infrastructure of the NLHPC (ECM-02) and ANID-PIA AFB 170001. Funding Information: The authors thank Dr. Juan C. Opazo for his technical support with the Phylogenetic Analysis by Maximum Likelihood (PAML) analysis. This work is part of the Chilean 1000 Genomes Initiative and is carried out within the framework of the Earth Biogenome Project (www.earthbiogenome.org). Funding has been provided by ANID/FONDAP 15090007 and 15200002, ANID/FONDECYT 1180606 (to MLA), ANID/FONDECYT 3190720 (to RMA) and ANID/FONDECYT 1200419 (to M Mendez). This research was partially supported by the supercomputing infrastructure of the NLHPC (ECM-02) and ANID-PIA AFB 170001. Publisher Copyright: © 2021

PY - 2022/1

Y1 - 2022/1

N2 - Orestias ascotanensis (Cyprinodontidae) is a teleost pupfish endemic to springs feeding into the Ascotan saltpan in the Chilean Altiplano (3,700 m.a.s.l.) and represents an opportunity to study adaptations to high-altitude aquatic environments. We have de novo assembled the genome of O. ascotanensis at high coverage. Comparative analysis of the O. ascotanensis genome showed an overall process of contraction, including loss of genes related to G-protein signaling, chemotaxis and signal transduction, while there was expansion of gene families associated with microtubule-based movement and protein ubiquitination. We identified 818 genes under positive selection, many of which are involved in DNA repair. Additionally, we identified novel and conserved microRNAs expressed in O. ascotanensis and its closely-related species, Orestias gloriae. Our analysis suggests that positive selection and expansion of genes that preserve genome stability are a potential adaptive mechanism to cope with the increased solar UV radiation to which high-altitude animals are exposed to.

AB - Orestias ascotanensis (Cyprinodontidae) is a teleost pupfish endemic to springs feeding into the Ascotan saltpan in the Chilean Altiplano (3,700 m.a.s.l.) and represents an opportunity to study adaptations to high-altitude aquatic environments. We have de novo assembled the genome of O. ascotanensis at high coverage. Comparative analysis of the O. ascotanensis genome showed an overall process of contraction, including loss of genes related to G-protein signaling, chemotaxis and signal transduction, while there was expansion of gene families associated with microtubule-based movement and protein ubiquitination. We identified 818 genes under positive selection, many of which are involved in DNA repair. Additionally, we identified novel and conserved microRNAs expressed in O. ascotanensis and its closely-related species, Orestias gloriae. Our analysis suggests that positive selection and expansion of genes that preserve genome stability are a potential adaptive mechanism to cope with the increased solar UV radiation to which high-altitude animals are exposed to.

KW - Altiplano

KW - Desert pupfish

KW - DNA repair

KW - High-altitude

KW - microRNAs

KW - Orestias ascotanensis

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SN - 0888-7543

VL - 114

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JO - Genomics

JF - Genomics

IS - 1

ER -

Genome sequencing and transcriptomic analysis of the Andean killifish Orestias ascotanensis reveals adaptation to high-altitude aquatic life

Abstract

Bibliographical note

Keywords

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