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Ectothermic vertebrates evolved gut-associated germinal center-like structures

ABSTRACT: Germinal centers (GCs), specialized microanatomical structures that emerged in endothermic vertebrates, serve as critical hubs for immune surveillance and lymphocyte activation. The constant exposure to foodborne pathogens drives the evolutionary selection for potent gut mucosal immune defenses in vertebrate species. Despite retaining ancestral ectothermic traits including underdeveloped lymph nodes, teleost fish have evolved specialized gut-associated lymphoid tissue capable of generating robust antigen-specific immune responses. How and where ectothermic vertebrates initiate adaptive immunity in the gut remains enigmatic. Through single-cell RNA sequencing (scRNA-seq), we comprehensively mapped the dynamic immune landscape of common carp (Cyprinus carpio) in the gut and head kidney (HK) following Spring Viremia of Carp Virus (SVCV) challenge. Strikingly, lymphocytes within gut exhibited pronounced upregulation of memory-related genes upon secondary viral exposure, oncomitant with robust expression of canonical GC markers in B cells. Furthermore, using FISH, we observed SVCV co-localization with CXCR5⁺ B cells within the lamina propria basement of the gut and perivascular niches of the HK, encircled by a peripheral ring of AICDA⁺/MKI67⁺/CXCR4⁺ B cells. Notably, within these same microanatomical niches, we detected distinct aggregates composed of highly proliferative IgM⁺ B cells undergoing significant apoptosis and antigen (Ag)-specific B cells. Collectively, our findings reveal that teleosts have evolved GC-like structures in the gut, offering novel insights into the evolutionary origins of GCs.

ORGANISM(S): Cyprinus carpio

PROVIDER: GSE299240 | GEO | 2026/06/06

REPOSITORIES: GEO

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Project description:In the last years, the innate immune response has gained importance since evidences indicate that, after an adequate priming protocol, it is possible to obtain some prolonged and enhanced immune response. Nevertheless, several factors, such as timing and method of administration of the immunostimulants need to be carefully considered. An inappropriate protocol can transform the treatments into a double-edged sword for the teleost immune system, resulting in a stressful and immunosuppressive status. In this work, we analyzed the long-term effect of different stimuli (β-glucans, lipopolysaccharide and Polyinosinic:polycytidylic acid) on the transcriptome modulation induced by Spring Viraemia Carp Virus (SVCV) in adult zebrafish (Danio rerio) and on the mortalities caused by this infection. At 35 days post-immunostimulation the transcriptome was found to be highly altered compared to the control fish, and these stimuli also conditioned the response to SVCV challenge, especially in the case of β-glucans. No protection against SVCV was found with any of the stimuli and even non-significant higher mortalities were observed, especially with β-glucans. However, at short-term (a pre-stimulation with β-glucan and infection after 7 days) a slight protection was observed after infection. The transcriptome response in zebrafish kidney at 35 days post-treatment with β-glucans revealed a significant response associated to stress and immunosuppression. The identification of genes differentially expressed before and after the infection seem to indicate a high energy cost of the immunostimulation prolonged in time that could explain the lack of protection against the SVCV. The differential response to stress, alterations in the lipid metabolism, the tryptophan-kynurenine pathway and the interferon-gamma signaling seem to be some of the mechanisms involved in this particular response, which means the end of the trained immunity and the beginning of a stressful status characterized by immunosuppression.

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Ectothermic vertebrates evolved gut-associated germinal center-like structures

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