Disparate developmental patterns of immune responses to bacterial and viral infections in fish.

Abdullah Alzaid,Samuel A M Martin,Rosario Castro,Christopher J Secombes,Daniel J Macqueen,Luc Jouneau,Luca Tacchi,Pierre Boudinot

doi:10.1038/srep15458

Abdullah Alzaid, Samuel A M Martin + Show 6 more

Open Access

https://doi.org/10.1038/srep15458

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Abstract

During early stages of development vertebrates rely on an immature immune system to fight pathogens, but in non mammalian species few studies have taken an in-depth analysis of the transition from reliance on innate immune mechanisms to the appearance of adaptive immunity. Using rainbow trout as a model we characterized responses to two natural pathogens of this species, the Gram negative bacterium Aeromonas salmonicida and the virus VHSV, using microarray analysis at four early life history stages; eyed egg, post hatch, first feeding and three weeks post first feeding when adaptive immunity starts to be effective. All stages responded to both infections, but the complexity of the response increased with developmental stage. The response to virus showed a clear interferon response only from first feeding. In contrast, bacterial infection induced a marked response from early stages, with modulation of inflammatory, antimicrobial peptide and complement genes across all developmental stages. Whilst the viral and bacterial responses were distinct, there were modulated genes in common, mainly of general inflammatory molecules. This work provides a first platform to explore the development of fish immunity to infection, and to compare the age-dependent changes (from embryo to adults) across vertebrates.

Highlights

During early stages of development vertebrates rely on an immature immune system to fight pathogens, but in non mammalian species few studies have taken an in-depth analysis of the transition from reliance on innate immune mechanisms to the appearance of adaptive immunity
We found at the time of first feeding that components of the acquired immune system become more responsive
Infections were performed in parallel either by bath or by injection with two pathogens, VHSV and A. salmonicida, for which comprehensive descriptions of infection-induced modifications of the transcriptome have been reported in adult tissues[16,18]

Summary

Introduction

During early stages of development vertebrates rely on an immature immune system to fight pathogens, but in non mammalian species few studies have taken an in-depth analysis of the transition from reliance on innate immune mechanisms to the appearance of adaptive immunity. In most non mammalian vertebrates, pre- and post- hatch life occurs in an unpredictable, hostile external environment This is in contrast to mammals where the embryo is in an almost sterile environment where pathogen exposure is controlled by the mother. Mouth and gut opening and first feeding stages represent another critical transition: as the gut microbiota is established[8], interactions between the developing teleost immune system and the environment intensify, increasing dramatically the need for efficient defence mechanisms against pathogens. Generic defence mechanisms like proinflammatory responses lead to wide cell activation, but pathogen www.nature.com/scientificreports/

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