Terrestrial adaptation: Expansion of myoglobin and up-regulation of hemoglobin genes in the walking catfish (Clarias batrachus)

Abstract

Walking catfish (Clarias batrachus), a freshwater fish capable of locomotion on land, serves as a great model for understanding adaptations to terrestrial life. Through comparative genome analysis, here I report that no genes were found within the walking catfish genome specifically related to the air-breathing capability. Instead, adaptive evolution was found in the C. batrachus genome to be involved in gene expression and nitrogenous waste metabolic process. Furthermore, myoglobin, olfactory receptor related to class A G protein-coupled receptor 1, and sulfotransferase 6b1 gene families were found specifically expanded in the air-breathing walking catfish genome with 15, 12, and 15 copies, respectively, while non-air-breathing fishes possess only 1-2 copies of these genes. Additionally, comparative transcriptome analysis between the air-breathing organ and the gill demonstrates the mechanism of aerial respiration involved in elastic fiber formation, oxygen binding and transport, and angiogenesis. Especially hemoglobin genes were expressed dramatically higher in the air-breathing organ than in the gill of C. batrachus. It is apparent that the coupling of enhanced abilities in oxygen transport and oxygen storage through genomic expansion of myoglobin and transcriptomic up-regulation of hemoglobin is an important component of the molecular basis for the adaptation of aquatic species to terrestrial life.