Research Article: Mucosal immunoglobulins protect the olfactory organ of teleost fish against parasitic infection

Date Published: November 5, 2018

Publisher: Public Library of Science

Author(s): Yong-Yao Yu, Weiguang Kong, Ya-Xing Yin, Fen Dong, Zhen-Yu Huang, Guang-Mei Yin, Shuai Dong, Irene Salinas, Yong-An Zhang, Zhen Xu, Daniel R. Barreda.

http://doi.org/10.1371/journal.ppat.1007251

Abstract

The olfactory organ of vertebrates receives chemical cues present in the air or water and, at the same time, they are exposed to invading pathogens. Nasal-associated lymphoid tissue (NALT), which serves as a mucosal inductive site for humoral immune responses against antigen stimulation in mammals, is present also in teleosts. IgT in teleosts is responsible for similar functions to those carried out by IgA in mammals. Moreover, teleost NALT is known to contain B-cells and teleost nasal mucus contains immunoglobulins (Igs). Yet, whether nasal B cells and Igs respond to infection remains unknown. We hypothesized that water-borne parasites can invade the nasal cavity of fish and elicit local specific immune responses. To address this hypothesis, we developed a model of bath infection with the Ichthyophthirius multifiliis (Ich) parasite in rainbow trout, Oncorhynchus mykiss, an ancient bony fish, and investigated the nasal adaptive immune response against this parasite. Critically, we found that Ich parasites in water could reach the nasal cavity and successfully invade the nasal mucosa. Moreover, strong parasite-specific IgT responses were detected in the nasal mucus, and the accumulation of IgT+ B-cells was noted in the nasal epidermis after Ich infection. Strikingly, local IgT+ B-cell proliferation and parasite-specific IgT generation were found in the trout olfactory organ, providing new evidence that nasal-specific immune responses were induced locally by a parasitic challenge. Overall, our findings suggest that nasal mucosal adaptive immune responses are similar to those reported in other fish mucosal sites and that an antibody system with a dedicated mucosal Ig performs evolutionary conserved functions across vertebrate mucosal surfaces.

Partial Text

Olfaction is a vital sense for all animals [1]. To receive an olfactory signal, terrestrial vertebrates inhale gases containing volatile chemical substances, while aquatic vertebrates like teleost fish actively draw water containing dissolved chemicals into the olfactory organs [2]. Simultaneously, during this process, the olfactory organs are constantly stimulated by toxins and pathogens in the air or water [3]. Therefore, there is an evident need to defend the large, delicate surface of olfactory organs from pathogenic invasion.

Protozoans are the most common parasites of freshwater and marine fish [27–29]. Ich is one of the most problematic parasites in freshwater ecosystems infecting many different fish species [30, 31]. Ich has been traditionally associated with skin and gill lesions in rainbow trout [15, 17], however, the teleost olfactory organ is constantly exposed to the aquatic environment and therefore may represent a route of entry for any pathogen. Here we report for the first time that Ich can infect the olfactory organ of rainbow trout when the fish are exposed to the parasite by bath, the natural route of exposure. Importantly, we found that parasite loads in the olfactory organ were the highest along with the gills, suggesting that the olfactory route of infection may be one of the main targets of this parasite. Given that the impacts of Ich invasion via the nose have until now been overlooked, further investigations are required to determine the impacts of Ich nasal infections in the fish host health.

 

Source:

http://doi.org/10.1371/journal.ppat.1007251