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Comparative Genomic and Transcriptomic Analyses Revealed Twenty-Six Candidate Genes Involved in the Air-Breathing Development and Function of the Bighead Catfish Clarias macrocephalus

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Abstract

The bighead catfish (Clarias macrocephalus) and channel catfish (Ictalurus punctatus) are freshwater species in the Siluriformes order. C. macrocephalus has both gills and modified gill structures serving as an air-breathing organ (ABO), while I. punctatus does not possess such an organ, and cannot breathe in air, providing an excellent model for studying the molecular basis of ABO development in teleost fish. To investigate the critical time window for the development of air-breathing function, seven development stages were selected based on hypoxia challenge results, and RNA-seq was performed upon C. macrocephalus to compare with the non-air-breathing I. punctatus. Five-hundred million reads were generated and 25,239 expressed genes were annotated in C. macrocephalus. Among those, 8675 genes were differentially expressed across developmental stages. Comparative genomic analysis identified 1458 C. macrocephalus specific genes, which were absent in I. punctatus. Gene network and protein-protein interaction analyses identified 26 key hub genes involved in the air-breathing function. Three top candidate genes, mb, ngb, hbae, are mainly associated with oxygen carrying, oxygen binding, and heme binding activities. Our study provides a rich data set for exploring the genomic basis of air-breathing function in C. macrocephalus and offers insights into the adaption to hypoxic environments.

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Data Availability

The raw RNA-seq data is available at NCBI GEO (Gene Expression Omnibus) databases under the accession number GSE151993.

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Acknowledgments

Ma, Xiaoli, a graduate student at School of Fisheries, Aquaculture, and Aquatic Sciences, Auburn University, was supported by the China Scholarship Council. X.W. is supported by Alabama Agricultural Experiment Station Enabling Grant, National Science Foundation EPSCoR RII Track-4 Research Fellowship (NSF OIA 1928770), the USDA National Institute of Food and Agriculture (Hatch project 1018100), and a generous laboratory start-up fund from Auburn University College of Veterinary Medicine. The authors would like to thank the Auburn Hopper supercomputer clusters for computational support.

Funding

This work was supported by an IGP grant (no. 180302) from the Auburn University Office of Vice President for Research.

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Authors and Affiliations

  1. School of Fisheries, Aquaculture and Aquatic Sciences, Auburn University, Auburn, AL, 36849, USA

    Xiaoli Ma, Baofeng Su, Max Bangs, Veronica Alston, Nathan J. C. Backenstose, Rhoda Mae Simora, Wenwen Wang, De Xing, Shangjia Li, Zhi Ye & Rex A. Dunham

  2. Alabama Agricultural Experiment Station, Auburn, AL, 36849, USA

    Xiaoli Ma, Baofeng Su, Max Bangs, Veronica Alston, Nathan J. C. Backenstose, Rhoda Mae Simora, Wenwen Wang, De Xing, Shangjia Li, Zhi Ye, Anthony G. Moss, Xu Wang & Rex A. Dunham

  3. Department of Biological Science, Florida State University, Tallahassee, FL, 32304, USA

    Max Bangs

  4. Department of Biological Sciences, University at Buffalo, Buffalo, NY, 14260, USA

    Nathan J. C. Backenstose

  5. College of Fisheries and Ocean Sciences, University of the Philippines Visayas, Miagao, 5023, Iloilo, Philippines

    Rhoda Mae Simora

  6. Department of Biochemistry, University of Washington, Seattle, WA, 98195, USA

    Zhi Ye

  7. Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA

    Anthony G. Moss

  8. College of Aquaculture and Fisheries, Can Tho University, Can Tho City, 94000, Vietnam

    Thuy-Yen Duong

  9. Department of Pathobiology, Auburn University, Auburn, AL, 36849, USA

    Xu Wang

  10. HudsonAlpha Institute for Biotechnology, Huntsville, AL, 35806, USA

    Xu Wang

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Ma, X., Su, B., Bangs, M. et al. Comparative Genomic and Transcriptomic Analyses Revealed Twenty-Six Candidate Genes Involved in the Air-Breathing Development and Function of the Bighead Catfish Clarias macrocephalus. Mar Biotechnol 23, 90–105 (2021). https://doi.org/10.1007/s10126-020-10005-4

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