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Mystifying Molecular Structure, Expression and Repertoire Diversity of IgM Heavy Chain Genes (Ighμ) in Clarias Catfish and Hybrids: Two Novel Transcripts in Vertebrates.

ABSTRACT: Two novel immunoglobulin heavy chain (Ighμ) transcripts encoding membrane-bound forms of IgM (mIgM) were discovered in bighead catfish, Clarias macrocephalus. The first transcript contains four constant and two transmembrane domains [Cμ1-Cμ2-Cμ3-Cμ4-TM1-TM2] that have never been reported in teleosts, and the second transcript is an unusual mIgM that has never been identified in any vertebrate [Cμ1-(Cδ2-Cδ3-Cδ4-Cδ5)-Cμ2-Cμ3-TM1-TM2]. Fluorescence in situ hybridization (FISH) in bighead catfish, North African catfish (C. gariepinus) and hybrid catfish revealed a single copy of Ighμ in individual parent catfish, while two gene copies were found in diploid hybrid catfish. Intensive sequence analysis demonstrated multiple distinct structural variabilities in the VH domain in Clarias, and hybrid catfish were defined and used to generate diversity with various mechanisms. Expression analysis of Ighμ in Aeromonas hydrophila infection of the head kidney, peripheral blood leukocytes and spleen revealed significantly higher levels in North African catfish and hybrid catfish than in bighead catfish.

SUBMITTER: Bunnoy A

PROVIDER: S-EPMC9247300 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Dataset Information

Mystifying Molecular Structure, Expression and Repertoire Diversity of IgM Heavy Chain Genes (Ighμ) in Clarias Catfish and Hybrids: Two Novel Transcripts in Vertebrates.

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