The emergence of the adaptive immune system in vertebrates set the stage for evolution of an advanced symbiotic relationship with the intestinal microbiota. The defining features of specificity and memory that characterize adaptive immunity have afforded vertebrates the mechanisms for efficiently tailoring immune responses to diverse types of microbes, whether to promote mutualism or host defence. These same attributes can put the host at risk of immune-mediated diseases that are increasingly linked to the intestinal microbiota. Understanding how the adaptive immune system copes with the remarkable number and diversity of microbes that colonize the digestive tract, and how the system integrates with more primitive innate immune mechanisms to maintain immune homeostasis, holds considerable promise for new approaches to modulate immune networks to treat and prevent disease.

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Reciprocal Interactions of the Intestinal Microbiota and Immune System

The vertebrate immune system is comprised of numerous distinct and interdependent components Every component has its own inherent protective value, and the final combination of them is likely to be related to an animal’s immunological history and evolutionary development Vertebrate immune system consists of both systemic and mucosal immune compartments, but it is the mucosal immune system which protects the body from the first encounter of pathogens According to anatomical location, the mucosa-associated lymphoid tissue, in teleost fish is subdivided into gut-, skin-, and gill-associated lymphoid tissue and most available studies focus on gut The purpose of this paper is to summarise the current knowledge of the immunological defences present in skin mucosa as a very important part of the fish immune system, serving as an anatomical and physiological barrier against external hazards Interest in defence mechanism of fish arises from a need to develop health management tools to support a growing finfish aquaculture industry, while at the same time addressing questions concerning origins and evolution of immunity in vertebrates Increased knowledge of fish mucosal immune system will facilitate the development of novel vaccination strategies in fish

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An Overview of the Immunological Defenses in Fish Skin

The mucosal immune system of fish: The evolution of tolerating commensals while fighting pathogens

To connect human biology to fish biomedical models, we sequenced the genome of spotted gar (Lepisosteus oculatus), whose lineage diverged from teleosts before teleost genome duplication (TGD). The slowly evolving gar genome has conserved in content and size many entire chromosomes from bony vertebrate ancestors. Gar bridges teleosts to tetrapods by illuminating the evolution of immunity, mineralization and development (mediated, for example, by Hox, ParaHox and microRNA genes). Numerous conserved noncoding elements (CNEs; often cis regulatory) undetectable in direct human-teleost comparisons become apparent using gar: functional studies uncovered conserved roles for such cryptic CNEs, facilitating annotation of sequences identified in human genome-wide association studies. Transcriptomic analyses showed that the sums of expression domains and expression levels for duplicated teleost genes often approximate the patterns and levels of expression for gar genes, consistent with subfunctionalization. The gar genome provides a resource for understanding evolution after genome duplication, the origin of vertebrate genomes and the function of human regulatory sequences.

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The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons

As physical barriers that separate teleost fish from the external environment, mucosae are also active immunological sites that protect them against exposure to microbes and stressors. In mammals, the sites where antigens are sampled from mucosal surfaces and where stimulation of naive T and B lymphocytes occurs are known as inductive sites and are constituted by mucosa-associated lymphoid tissue (MALT). According to anatomical location, the MALT in teleost fish is subdivided into gut-associated lymphoid tissue (GALT), skin-associated lymphoid tissue (SALT), and gill-associated lymphoid tissue (GIALT). All MALT contain a variety of leukocytes, including, but not limited to, T cells, B cells, plasma cells, macrophages and granulocytes. Secretory immunoglobulins are produced mainly by plasmablasts and plasma cells, and play key roles in the maintenance of mucosal homeostasis. Until recently, teleost fish B cells were thought to express only two classes of immunoglobulins, IgM and IgD, in which IgM was thought to be the only one responding to pathogens both in systemic and mucosal compartments. However, a third teleost immunoglobulin class, IgT/IgZ, was discovered in 2005, and it has recently been shown to behave as the prevalent immunoglobulin in gut mucosal immune responses. The purpose of this review is to summarise the current knowledge of mucosal immunoglobulins and B cells of fish MALT. Moreover, we attempt to integrate the existing knowledge on both basic and applied research findings on fish mucosal immune responses, with the goal to provide new directions that may facilitate the development of novel vaccination strategies that stimulate not only systemic, but also mucosal immunity.

/pdf/mucosal-immunoglobulins-and-b-cells-of-teleost-fish-8zdjg1g1cr.pdf

Mucosal immunoglobulins and B cells of teleost fish

Teleost fish are the most primitive bony vertebrates that contain immunoglobulins. In contrast to mammals and birds, these species are devoid of immunoglobulin A (IgA) or a functional equivalent. This observation suggests that specialization of immunoglobulin isotypes into mucosal and systemic responses took place during tetrapod evolution. Challenging that paradigm, here we show that IgT, an immunoglobulin isotype of unknown function, acts like a mucosal antibody. We detected responses of rainbow trout IgT to an intestinal parasite only in the gut, whereas IgM responses were confined to the serum. IgT coated most intestinal bacteria. As IgT and IgA are phylogenetically distant immunoglobulins, their specialization into mucosal responses probably occurred independently by a process of convergent evolution.

/pdf/igt-a-primitive-immunoglobulin-class-specialized-in-mucosal-1jobfp961d.pdf

IgT, a primitive immunoglobulin class specialized in mucosal immunity

Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts

Ceratomyxa shasta infects salmon and trout, causing ceratomyxosis, a disease charac- terized by parasite proliferation in the intestine and death. We used laboratory challenges to investi- gate the infective dose for 3 fish species: a susceptible strain of rainbow trout Oncorhynchus mykiss and comparatively resistant Chinook O. tshawytscha and coho salmon O. kisutch. For susceptible rainbow trout, we determined the outcome of infection under conditions of varying parasite dose, fish size, and parasite concentration. A single actinospore was sufficient to cause a lethal infection in sus- ceptible rainbow trout. The mean days to death (MDD) did not significantly decrease among doses causing 100% prevalence, indicating a minimum time required for parasites to replicate to a fatal level. When dose was constant, but delivered in a higher parasite concentration, higher infection prevalence and mortality resulted. One actinospore fish -1 caused 57% infection and mortality in fish challenged in 0.5 l of water, whereas 10 spores fish -1 resulted in an average of 49% infection and mortality in 1 l challenges. This effect is most likely due to a higher encounter rate in the smaller water volume. Neither infection prevalence nor MDD was significantly different between large trout (84.9 g) and small trout (6.3 g). Chinook salmon did not become infected even when challenged with 5000 actinospores. One fatal infection occurred in coho salmon challenged with 1000 actinospores. This study confirms that even low doses of C. shasta cause severe infection in highly susceptible fish, describes the dose response on MDD, and demonstrates that parasite concentration influences infec- tion prevalence.

/pdf/effects-of-ceratomyxa-shasta-dose-on-a-susceptible-strain-of-1xuj4muypl.pdf

Effects of Ceratomyxa shasta dose on a susceptible strain of rainbow trout and comparatively resistant Chinook and coho salmon.

Ceratomyxa shasta is a myxozoan parasite identified as a contributor to salmon mortality in the Klamath River, USA The parasite has a complex life cycle involving a freshwater polychaete, Manayunkia speciosa and a salmonid As part of ongoing research on how environmental parameters influence parasite establishment and replication, we designed a laboratory experiment to examine the effect of water flow (velocity) on completion of the C shasta infectious cycle The experiment tested the effect of two water velocities, 005 and 001 m s(-1), on survival and infection of M speciosa as well as transmission to susceptible rainbow trout and comparatively resistant Klamath River Chinook salmon The faster water velocity facilitated the greatest polychaete densities, but the lowest polychaete infection prevalence Rainbow trout became infected in all treatments, but at the slower velocity had a shorter mean day to death, indicating a higher infectious dose Infection was not detected in Chinook salmon even at a dose estimated to be as high as 80,000 actinospores per fish The higher water velocity resulted in lower C shasta infection prevalence in M speciosa and decreased infection severity in fish Another outcome of our experiment is the description of a system for maintaining and infecting M speciosa in the laboratory

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The effects of water velocity on the Ceratomyxa shasta infectious cycle.

https://ir.library.oregonstate.edu/downloads/cj82k9346

Sarah J. Bjork

Papers

IgT, a primitive immunoglobulin class specialized in mucosal immunity

Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts

Effects of Ceratomyxa shasta dose on a susceptible strain of rainbow trout and comparatively resistant Chinook and coho salmon.

The effects of water velocity on the Ceratomyxa shasta infectious cycle.

Defenses of susceptible and resistant Chinook salmon (Onchorhynchus tshawytscha) against the myxozoan parasite Ceratomyxa shasta