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

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.

Gut mucosal immune responses and protective efficacy of oral yeast Cyprinid herpesvirus 2 (CyHV-2) vaccine in Carassius auratus gibelio

“…Similar to the previous study (70), here the expression of igt was much higher than that of igm in the gut, and in systemic tissues, the expression level of igm was significantly higher than that of igt. Moreover, similar to our study, the expression of igt in the hindgut was significantly stronger than that in the spleen or head kidney after vaccination with an oral vaccine against IHNV (71), virus-specific IgM and IgT were found to be significantly elevated in systemic and mucosal tissues, respectively, in rainbow trout after infection with IHNV (72). In addition to the potential complementary role of IgD to canonical mucosal IgT and IgM responses, IgD may establish a mutualistic relationship with commensals to enhance mucosal homeostasis (73).…”

Gallbladder microbiota in early vertebrates provides evolutionary insights into mucosal homeostasis

“…To investigate whether viral infection can generate a GB immune response in teleost fish and assess the changes in the microbial structure of the bile environment, we established an infection model by immersion with IHNV, which is a fatal Novirhabdovirus that affects salmonid species including rainbow trout. Importantly, we have previously demonstrated that IHNV can invade the internal organs of rainbow trout, including the gut and swim bladder ( 17 , 20 ). Using our previously reported immersion infection approach, our study demonstrated that IHNV can reach the GB organ through BL circulation and induce high expression levels of the stat1 , mx1 , lgp2 , tirm25 , rag1 , ifnar , and mda5 genes, all of which have been associated with antiviral immunity ( 39 – 43 ).…”

“…The supernatant containing IHNV was filtered with a 0.22 μm PES membrane filtration (Millipore) to remove bacteria, and titrated by the Median Tissue Culture Infectious Dose (TCID 50 ) assay on EPC cells following the methodology reported by Yu et al. ( 17 ).…”

“…Trout GB were fixed in 4% neutral buffered formalin overnight at 4°, paraffin embedded, and 5 μm thick sections stained with hematoxylin-eosin (H & E) and Alcian Blue-Periodic acid-schiff (AB-PAS) as described previously ( 17 ). Images were acquired by a microscope (Olympus).…”

“…When extensive cytopathic effects (CPEs) were observed, the infected cells were collected, and followed by a gradient centrifugation (400 g for 10 min, 3,000 g for 10 min, and 10,000 g for 10 min) to remove the cells debris. The supernatant containing IHNV was filtered with a 0.22 mm PES membrane filtration (Millipore) to remove bacteria, and titrated by the Median Tissue Culture Infectious Dose (TCID 50 ) assay on EPC cells following the methodology reported by Yu et al (17).…”