Estensoro Itziar, López-Gurillo Beatriz, Tafalla Carolina, Craig Ryan, Atkinson Stephen, Sitjà-Bobadilla Ariadna, Bartholomew Jerri
Fish Pathology Group, Instituto de Acuicultura Torre de la Sal, Consejo Superior de Investigaciones Científicas (IATS, CSIC), Castellón, Spain.
Biotechnology Department, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain.
Front Cell Infect Microbiol. 2025 Jun 27;15:1576014. doi: 10.3389/fcimb.2025.1576014. eCollection 2025.
Ceratomyxosis due to the myxozoan parasite affects salmonids, causing severe enteritis leading to hemorrhaging and necrosis. The waterborne parasite stages penetrate host gills and reach the fish intestine through the bloodstream. Steelhead trout () populations from endemic watersheds (sympatric) are less susceptible than populations from non-endemic watersheds (allopatric). We investigated the immune effectors behind these different susceptibilities. Both steelhead trout strains were exposed to genotype 0. Intestinal tissue and serum samples of control and exposed sympatric and allopatric fish were taken at 8, 15, 22, 29, 57, and 183 days post exposure. Gills were taken at 1 and 8 days post exposure. Parasite abundance and histopathology were evaluated on tissue sections of fish that tested PCR+ for the parasite. Zap70 T cells, IgT B cells, and IgD B cells were quantified, and the presence of specific IgM was evaluated from fish sera by immunohistochemistry. Parasite counts were significantly lower and limited to a shorter duration in sympatric fish. The initial intestinal inflammatory response in both fish strains was characterized by hyperplasia of the lamina propria-submucosa and epithelial infiltration of lymphocytes. Remarkably, hyperplasia was resolved earlier in sympatric fish, whereas in allopatric fish, hyperplasia was not resolved by the end of the experiment, coinciding with high intestinal parasite counts and sporogenesis. An increase of intestinal Zap70 T cells occurred before IgT B cells peaked, earlier in sympatric than in allopatric fish. Low numbers of intestinal IgD B cells were detected in both strains. In gills, an early increase of Zap70 T cells was observed in both fish strains at 1 day post exposure, and an increase of IgD B cells occurred only in the allopatric strain. Specific circulating IgM was detected much later in both fish strains, only at 57 and 183 days post exposure. In conclusion, sympatric steelhead trout restricted intestinal proliferation of genotype 0 more effectively than allopatric fish, probably due to an earlier T cell response triggering a stronger IgT-based mucosal adaptive response in the intestine. Specific circulating IgM appeared later in both sympatric and allopatric fish, probably also contributing systemic protection.
由粘孢子虫寄生虫引起的角孢子虫病会影响鲑科鱼类，导致严重的肠炎，进而引发出血和坏死。寄生虫的水传播阶段穿透宿主鳃，并通过血液循环到达鱼的肠道。来自地方性流域（同域分布）的虹鳟鱼种群比来自非地方性流域（异域分布）的种群更不易感。我们研究了这些不同易感性背后的免疫效应器。将两种虹鳟鱼品系都暴露于基因型0。在暴露后第8、15、22、29、57和183天采集对照以及暴露后的同域和异域鱼类的肠道组织和血清样本。在暴露后第1天和第8天采集鳃样本。对经PCR检测寄生虫呈阳性的鱼的组织切片进行寄生虫丰度和组织病理学评估。对Zap70 T细胞、IgT B细胞和IgD B细胞进行定量，并通过免疫组织化学从鱼血清中评估特异性IgM的存在。同域鱼类中的寄生虫数量显著更低，且局限于更短的持续时间。两种鱼品系最初的肠道炎症反应特征为固有层 - 黏膜下层增生以及淋巴细胞的上皮浸润。值得注意的是，同域鱼类中的增生更早得到缓解，而异域鱼类在实验结束时增生仍未缓解，这与肠道寄生虫数量高和孢子形成同时发生。肠道Zap70 T细胞的增加发生在IgT B细胞达到峰值之前，同域鱼类比异域鱼类更早出现。在两种品系中均检测到数量较少的肠道IgD B细胞。在鳃中，两种鱼品系在暴露后第1天均观察到Zap70 T细胞早期增加，而IgD B细胞的增加仅出现在异域品系中。两种鱼品系中特异性循环IgM在更晚的时候才被检测到，仅在暴露后第57天和第183天。总之，同域虹鳟鱼比异域鱼类更有效地限制了基因型0在肠道中的增殖，这可能是由于更早的T细胞反应触发了肠道中更强的基于IgT的黏膜适应性反应。特异性循环IgM在同域和异域鱼类中出现得都较晚，可能也有助于全身保护。
