Comparative Transcriptome Analysis During the Seven Developmental Stages of Channel Catfish (Ictalurus punctatus) and Tra Catfish (Pangasianodon hypophthalmus) Provides Novel Insights for Terrestrial Adaptation.

Xiaoli Ma,Anthony G Moss,Nathan J C Backenstose,Rhoda Mae Simora,Rex A Dunham,Baofeng Su,Mei Shang,Thuy-Yen Duong,Veronica Alston,Mai Thi Nguyen,Max Bangs,Xu Wang,Anne Wiley

doi:10.3389/fgene.2020.608325

Abstract

Tra catfish (Pangasianodon hypophthalmus), also known as striped catfish, is a facultative air-breather that uses its swim bladder as an air-breathing organ (ABO). A related species in the same order (Siluriformes), channel catfish (Ictalurus punctatus), does not possess an ABO and thus cannot breathe in the air. Tra and channel catfish serve as great comparative models for investigating possible genetic underpinnings of aquatic to land transitions, as well as for understanding genes that are crucial for the development of the swim bladder and the function of air-breathing in tra catfish. In this study, hypoxia challenge and microtomy experiments collectively revealed critical time points for the development of the air-breathing function and swim bladder in tra catfish. Seven developmental stages in tra catfish were selected for RNA-seq analysis based on their transition to a stage that could live at 0 ppm oxygen. More than 587 million sequencing clean reads were generated, and a total of 21,448 unique genes were detected. A comparative genomic analysis between channel catfish and tra catfish revealed 76 genes that were present in tra catfish, but absent from channel catfish. In order to further narrow down the list of these candidate genes, gene expression analysis was performed for these tra catfish-specific genes. Fourteen genes were inferred to be important for air-breathing. Of these, HRG, GRP, and CX3CL1 were identified to be the most likely genes related to air-breathing ability in tra catfish. This study provides a foundational data resource for functional genomic studies in air-breathing function in tra catfish and sheds light on the adaptation of aquatic organisms to the terrestrial environment.

Highlights

Oxygen is indispensable for all aerobic creatures
From the previous histology experiment, we investigated that the swim bladder can be observed in tra catfish larvae from 6 dpf, and the 0-ppm oxygen challenge experiment revealed that tra catfish larvae already possessed partial aerial breathing ability even before that
Fractalkine-like isoform X1 (CX3CL1) is another gene we identified in our developmental time series analysis, which is potentially important in the development of swim bladder and air-breathing function

Summary

Introduction

Oxygen is indispensable for all aerobic creatures. For animals, breathing is a critical biophysical and voluntary process that involves the uptake of oxygen and transferring it to the cells. For fish that receive oxygen from their surrounding aquatic environment, gills serve as the primary site for gas exchange (Palzenberger and Pohla, 1992). In addition to their respiratory function, gills serve as a pathway for the exchange of non-volatile molecules between the blood and the environment, and most fish exchange gases through gills that are protected under an operculum on both sides of the pharynx (Olson, 1991). The membrane creates small diffusion distances for gases and decreases branchial vascular resistance and increases the respiratory surface area, resulting in high diffusion capacity in air-breathing fish and improved respiratory efficiency, allowing such fish to survive even being exposed to air (Maina, 2002)

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