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Apr 05, 2022;8 (1): 31.

Teleost swim bladder, an ancient air-filled organ that elicits mucosal immune responses.

Yongyao Yu, Zhenyu Huang, Weiguang Kong, Fen Dong, Xiaoting Zhang, Xue Zhai, Gaofeng Cheng, Mengting Zhan, Jiafeng Cao, Liguo Ding, Guangkun Han, Fumio Takizawa, Yang Ding, J Oriol Sunyer, Zhen Xu
Author Information
  1. Yongyao Yu: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China. ORCID
  2. Zhenyu Huang: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  3. Weiguang Kong: State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, China.
  4. Fen Dong: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  5. Xiaoting Zhang: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  6. Xue Zhai: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  7. Gaofeng Cheng: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  8. Mengting Zhan: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  9. Jiafeng Cao: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  10. Liguo Ding: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  11. Guangkun Han: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China.
  12. Fumio Takizawa: Faculty of Marine Science and Technology, Fukui Prefectural University, Obama, Fukui, Japan.
  13. Yang Ding: Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, PA, USA.
  14. J Oriol Sunyer: Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, PA, USA. sunyer@vet.upenn.edu.
  15. Zhen Xu: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei, China. zhenxu@ihb.ac.cn.
PMID: 35379790 DOI: 10.1038/s41421-022-00393-3

Abstract

The air-filled organs (AOs) of vertebrates (lungs and swim bladders) have evolved unique functions (air-breathing or buoyancy control in water) to adapt to different environments. Thus far, immune responses to microbes in AOs have been described exclusively in the lungs of tetrapods. Similar to lungs, swim bladders (SBs) represent a mucosal surface, a feature that leads us to hypothesize a role for SB in immunity. In this study, we demonstrate that secretory IgT (sIgT) is the key SB immunoglobulin (Ig) responding to the viral challenge, and the only Ig involved in viral neutralization in that organ. In support of these findings, we found that the viral load of the SB from fish devoid of sIgT was much higher than that of control fish. Interestingly, similar to the lungs in mammals, the SB represents the mucosal surface in fish with the lowest content of microbiota. Moreover, sIgT is the main Ig class found coating their surface, suggesting a key role of this Ig in the homeostasis of the SB microbiota. In addition to the well-established role of SB in buoyancy control, our findings reveal a previously unrecognized function of teleost SB in adaptive mucosal immune responses upon pathogenic challenge, as well as a previously unidentified role of sIgT in antiviral defense. Overall, our findings indicate that despite the phylogenetic distance and physiological roles of teleost SB and mammalian lungs, they both have evolved analogous mucosal immune responses against microbes which likely originated independently through a process of convergent evolution.

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Grants

  1. R01 GM085207/NIGMS NIH HHS
  2. U1905204, 31873045, 32073001/National Natural Science Foundation of China (National Science Foundation of China)
Journal Article
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