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

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

doi:10.1186/s12864-018-5355-9

Abstract

BackgroundWalking 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.ResultsComparative 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.ConclusionsThis 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.

Highlights

Walking catfish (Clarias batrachus) is a freshwater fish capable of air-breathing and locomotion on land
The assembly covered a total of 821 Mb, similar to the genome size of 854 Mb estimated from ALLPATHS-LG, but slightly smaller than the estimated 900 Mb based on the Feulgen densitometry method [17] and the 1.17 Gb based on the bulk fluorometric assay method [18]
As our objective was to identify additional gene copies or novel genes in the walking catfish not found in non-air-breathing fishes, which may account for its adaptations for partial living on land, this level of completeness is reasonable, a small percentage of missing genes may reduce the capacity of identifying more such genes

Summary

Introduction

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 been thought to be damaging to native fish populations; there is little evidence to support this except that they do invade aquaculture facilities and can cause severe damage to cultured fish populations (Florida Museum, University of Florida 2017; https://www.floridamuseum.ufl.edu/fish/discover/species-profiles/clarias-batrachus/). Their air breathing capability allows them to disperse quickly across terrestrial environments, a feature that most native fish do not have

Objectives

Methods

Results

Discussion

Conclusion