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Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation

BACKGROUND: Walking catfish (Clarias batrachus) is a freshwater fish capable of air-breathing and locomotion on land. It usually inhabits various low-oxygen habitats, burrows inside the mudflat, and sometimes “walks” to search for suitable environments during summer. It has evolved accessory air-bre...

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Autores principales: Li, Ning, Bao, Lisui, Zhou, Tao, Yuan, Zihao, Liu, Shikai, Dunham, Rex, Li, Yuanning, Wang, Kun, Xu, Xiaoyan, Jin, Yulin, Zeng, Qifan, Gao, Sen, Fu, Qiang, Liu, Yang, Yang, Yujia, Li, Qi, Meyer, Axel, Gao, Dongya, Liu, Zhanjiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6302426/
https://www.ncbi.nlm.nih.gov/pubmed/30572844
http://dx.doi.org/10.1186/s12864-018-5355-9
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author Li, Ning
Bao, Lisui
Zhou, Tao
Yuan, Zihao
Liu, Shikai
Dunham, Rex
Li, Yuanning
Wang, Kun
Xu, Xiaoyan
Jin, Yulin
Zeng, Qifan
Gao, Sen
Fu, Qiang
Liu, Yang
Yang, Yujia
Li, Qi
Meyer, Axel
Gao, Dongya
Liu, Zhanjiang
author_facet Li, Ning
Bao, Lisui
Zhou, Tao
Yuan, Zihao
Liu, Shikai
Dunham, Rex
Li, Yuanning
Wang, Kun
Xu, Xiaoyan
Jin, Yulin
Zeng, Qifan
Gao, Sen
Fu, Qiang
Liu, Yang
Yang, Yujia
Li, Qi
Meyer, Axel
Gao, Dongya
Liu, Zhanjiang
author_sort Li, Ning
collection PubMed
description BACKGROUND: Walking catfish (Clarias batrachus) is a freshwater fish capable of air-breathing and locomotion on land. It usually inhabits various low-oxygen habitats, burrows inside the mudflat, and sometimes “walks” to search for suitable environments during summer. It has evolved accessory air-breathing organs for respiring air and corresponding mechanisms to survive in such challenging environments. Thereby, it serves as a great model for understanding adaptations to terrestrial life. RESULTS: Comparative genomics with channel catfish (Ictalurus punctatus) revealed specific adaptations of C. batrachus in DNA repair, enzyme activator activity, and small GTPase regulator activity. Comparative analysis with 11 non-air-breathing fish species suggested adaptive evolution in gene expression and nitrogenous waste metabolic processes. Further, myoglobin, olfactory receptor related to class A G protein-coupled receptor 1, and sulfotransferase 6b1 genes were found to be expanded in the air-breathing walking catfish genome, with 15, 15, and 12 copies, respectively, compared to non-air-breathing fishes that possess only 1–2 copies of these genes. Additionally, we sequenced and compared the transcriptomes of the gill and the air-breathing organ to characterize the mechanism of aerial respiration involved in elastic fiber formation, oxygen binding and transport, angiogenesis, ion homeostasis and acid-base balance. The hemoglobin genes were expressed dramatically higher in the air-breathing organ than in the gill of walking catfish. CONCLUSIONS: This study provides an important genomic resource for understanding the adaptive mechanisms of walking catfish to terrestrial environments. It is possible that the coupling of enhanced abilities for oxygen storage and oxygen transport through genomic expansion of myoglobin genes and transcriptomic up-regulation of hemoglobin and angiogenesis-related genes are important components of the molecular basis for adaptation of this aquatic species to terrestrial life. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5355-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-63024262018-12-31 Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation Li, Ning Bao, Lisui Zhou, Tao Yuan, Zihao Liu, Shikai Dunham, Rex Li, Yuanning Wang, Kun Xu, Xiaoyan Jin, Yulin Zeng, Qifan Gao, Sen Fu, Qiang Liu, Yang Yang, Yujia Li, Qi Meyer, Axel Gao, Dongya Liu, Zhanjiang BMC Genomics Research Article BACKGROUND: Walking catfish (Clarias batrachus) is a freshwater fish capable of air-breathing and locomotion on land. It usually inhabits various low-oxygen habitats, burrows inside the mudflat, and sometimes “walks” to search for suitable environments during summer. It has evolved accessory air-breathing organs for respiring air and corresponding mechanisms to survive in such challenging environments. Thereby, it serves as a great model for understanding adaptations to terrestrial life. RESULTS: Comparative genomics with channel catfish (Ictalurus punctatus) revealed specific adaptations of C. batrachus in DNA repair, enzyme activator activity, and small GTPase regulator activity. Comparative analysis with 11 non-air-breathing fish species suggested adaptive evolution in gene expression and nitrogenous waste metabolic processes. Further, myoglobin, olfactory receptor related to class A G protein-coupled receptor 1, and sulfotransferase 6b1 genes were found to be expanded in the air-breathing walking catfish genome, with 15, 15, and 12 copies, respectively, compared to non-air-breathing fishes that possess only 1–2 copies of these genes. Additionally, we sequenced and compared the transcriptomes of the gill and the air-breathing organ to characterize the mechanism of aerial respiration involved in elastic fiber formation, oxygen binding and transport, angiogenesis, ion homeostasis and acid-base balance. The hemoglobin genes were expressed dramatically higher in the air-breathing organ than in the gill of walking catfish. CONCLUSIONS: This study provides an important genomic resource for understanding the adaptive mechanisms of walking catfish to terrestrial environments. It is possible that the coupling of enhanced abilities for oxygen storage and oxygen transport through genomic expansion of myoglobin genes and transcriptomic up-regulation of hemoglobin and angiogenesis-related genes are important components of the molecular basis for adaptation of this aquatic species to terrestrial life. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5355-9) contains supplementary material, which is available to authorized users. BioMed Central 2018-12-20 /pmc/articles/PMC6302426/ /pubmed/30572844 http://dx.doi.org/10.1186/s12864-018-5355-9 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Li, Ning
Bao, Lisui
Zhou, Tao
Yuan, Zihao
Liu, Shikai
Dunham, Rex
Li, Yuanning
Wang, Kun
Xu, Xiaoyan
Jin, Yulin
Zeng, Qifan
Gao, Sen
Fu, Qiang
Liu, Yang
Yang, Yujia
Li, Qi
Meyer, Axel
Gao, Dongya
Liu, Zhanjiang
Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation
title Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation
title_full Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation
title_fullStr Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation
title_full_unstemmed Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation
title_short Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation
title_sort genome sequence of walking catfish (clarias batrachus) provides insights into terrestrial adaptation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6302426/
https://www.ncbi.nlm.nih.gov/pubmed/30572844
http://dx.doi.org/10.1186/s12864-018-5355-9
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