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

Ning Li, Lisui Bao, Tao Zhou, Zihao Yuan, Shikai Liu, Rex Dunham, Yuanning Li, Kun Wang, Xiaoyan Xu, Yulin Jin, Qifan Zeng, Sen Gao, Qiang Fu, Yang Liu, Yujia Yang, Qi Li, Axel Meyer, Dongya Gao, Zhanjian "John" Liu

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Article number952
JournalBMC Genomics
Volume19
Issue number1
DOIs
StatePublished - Dec 20 2018

Fingerprint

Catfishes
Walking
Respiration
Genome
Air
Ictaluridae
Oxygen
Fishes
Myoglobin
Genes
Hemoglobins
Odorant Receptors
Enzyme Activators
DNA Repair Enzymes
Gene Components
Sulfotransferases
Elastic Tissue
Monomeric GTP-Binding Proteins
Acid-Base Equilibrium
Ion Transport

Keywords

  • Adaptation
  • Air-breathing organ
  • Duplication
  • Evolution
  • Fish
  • Genome

ASJC Scopus subject areas

  • Biotechnology
  • Genetics

Cite this

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, Zhanjian "John".

In: BMC Genomics, Vol. 19, No. 1, 952, 20.12.2018.

Research output: Contribution to journalArticle

Li, N, Bao, L, Zhou, T, Yuan, Z, Liu, S, Dunham, R, Li, Y, Wang, K, Xu, X, Jin, Y, Zeng, Q, Gao, S, Fu, Q, Liu, Y, Yang, Y, Li, Q, Meyer, A, Gao, D & Liu, ZJ 2018, 'Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation', BMC Genomics, vol. 19, no. 1, 952. https://doi.org/10.1186/s12864-018-5355-9
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, Zhanjian "John". / Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation. In: BMC Genomics. 2018 ; Vol. 19, No. 1.
@article{22a9c6b5a93a43d8ba98ea2aae69e17a,
title = "Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation",
abstract = "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.",
keywords = "Adaptation, Air-breathing organ, Duplication, Evolution, Fish, Genome",
author = "Ning Li and Lisui Bao and Tao Zhou and Zihao Yuan and Shikai Liu and Rex Dunham and Yuanning Li and Kun Wang and Xiaoyan Xu and Yulin Jin and Qifan Zeng and Sen Gao and Qiang Fu and Yang Liu and Yujia Yang and Qi Li and Axel Meyer and Dongya Gao and Liu, {Zhanjian {"}John{"}}",
year = "2018",
month = "12",
day = "20",
doi = "10.1186/s12864-018-5355-9",
language = "English (US)",
volume = "19",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "BioMed Central",
number = "1",

}

TY - JOUR

T1 - Genome sequence of walking catfish (Clarias batrachus) provides insights into terrestrial adaptation

AU - Li, Ning

AU - Bao, Lisui

AU - Zhou, Tao

AU - Yuan, Zihao

AU - Liu, Shikai

AU - Dunham, Rex

AU - Li, Yuanning

AU - Wang, Kun

AU - Xu, Xiaoyan

AU - Jin, Yulin

AU - Zeng, Qifan

AU - Gao, Sen

AU - Fu, Qiang

AU - Liu, Yang

AU - Yang, Yujia

AU - Li, Qi

AU - Meyer, Axel

AU - Gao, Dongya

AU - Liu, Zhanjian "John"

PY - 2018/12/20

Y1 - 2018/12/20

N2 - 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.

AB - 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.

KW - Adaptation

KW - Air-breathing organ

KW - Duplication

KW - Evolution

KW - Fish

KW - Genome

UR - http://www.scopus.com/inward/record.url?scp=85058908226&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85058908226&partnerID=8YFLogxK

U2 - 10.1186/s12864-018-5355-9

DO - 10.1186/s12864-018-5355-9

M3 - Article

VL - 19

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 952

ER -