Elsevier

Fish & Shellfish Immunology

Volume 58, November 2016, Pages 33-41
Fish & Shellfish Immunology

Full length article
Smoltification and seawater transfer of Atlantic salmon (Salmo salar L.) is associated with systemic repression of the immune transcriptome

https://doi.org/10.1016/j.fsi.2016.09.026Get rights and content

Highlights

  • Smoltification of salmon is associated with profound endocrine alterations.

  • High incidence of infectious diseases in the sea indicate weakened protection.

  • Microarray analyses in head kidney, intestine and gill revealed immune suppression.

  • No recovery was observed after three weeks in seawater.

  • Duration and consequences of immune suppression need further exploration.

Abstract

Smoltification and seawater adaptation of Atlantic salmon are associated with profound alterations in the endocrine status, osmoregulation and behaviour. Little is known about immunological changes during smoltification, although increased incidences of infectious diseases after seawater transfer (SWT) may indicate weakened protection. We report microarray gene expression analyses in farmed Atlantic salmon during smoltification stimulated with constant light and early seawater adaptation (one and three weeks after SWT). Gene expression changes were large, their magnitude in the head kidney and proximal intestine was greater than in the gill. Among 360 differentially expressed immune genes, 300 genes were down-regulated, and multiple functional groups were affected such as innate antiviral immunity, chemokines, cytokines and receptors, signal transducers, effectors of humoral and cellular innate immunity, antigen presentation and lymphocytes, especially T cells. No recovery was observed after three weeks in seawater. A notable exception was a transient up-regulation of immunoglobulin transcripts in the gill after SWT. Genes involved in stress responses and xenobiotic metabolism were up-regulated in respectively intestine and gill. The duration of this observed immune suppression and the possible consequences for susceptibility to infections and diseases need further exploration.

Introduction

The life cycle of anadromous salmonids consists of fresh- and seawater phases, separated by parr–smolt transformation or smoltification that precedes migration to the sea. Smoltification begins when fish achieves an appropriate size being triggered by changes in photoperiod and water temperature. Major alterations in pituitary, thyroid and inter-renal tissues [1], [2] stimulate multiple changes including osmoregulation and enhanced salinity tolerance, higher metabolic rate, downstream migratory and schooling behaviour, decrease of condition factor, silvering, and olfactory imprinting [3]. Atlantic salmon aquaculture manipulates smoltification with an aid of artificial photoperiod to provide flexible production of smolts. Parr-smolt transformation and preparedness to seawater transfer (SWT) are monitored by fish appearance (silvering and body shape), enzymatic activity and expression of freshwater and seawater isoforms of Na+/K + ATPase and concentration of plasma chloride after exposure to seawater. SWT is a critical period in salmon life and the production cycle of aquaculture; a major part of the losses takes place during the first months in the sea [4]. SWT is commonly followed with augmented occurrence of diseases or sub-clinical infections with viral pathogens such as infectious pancreatic necrosis virus (causing infectious pancreas necrosis IPN) [5], salmonid alphaviruses (causing pancreas disease PD) [6], piscine myocarditis virus (causing cardiomyopathy syndrome CMS) [7], [8] and piscine orthoreovirus (causing heart and skeletal muscle inflammation HSMI) [9]. Bacterial and parasitic infections such as Moritella viscosa, Tenacibaculum and Parvicapsula pseudobranchiola are also associated with increasing morbidity or mortality post SWT in certain regions of Norway [10]. Increase of morbidity can be associated with multiple factors including greater pathogen pressure in the marine environment, combining of smolt batches from different hatcheries, stress and compromised immune protection. Until present, studies of parr-smolt transformation have focused mainly on endocrinology, osmoregulation and behaviour [3], [11], [12], while little is known about immunological changes during this process. We report transcriptome analyses in organs of Atlantic salmon that are in direct contact with seawater (gills and proximal intestine) and the primary immune and hematopoietic organ (head kidney).

Section snippets

Fish, smoltification and SWT

The experiment was performed 9. October -20. November (annual weeks 41–47) 2012 at The Aquaculture Research Station (Kårvika, Tromsø, Norway) The experiment was approved by the Norwegian animal research authority. The fish were treated according to Norwegian legislation and anesthetized prior to handling with Benzoak (benzocaine; 0.1 mg/ml) or euthanized with an overdose.

of Benzoak prior to all samplings. A total of 80 Atlantic salmon from the Aqua Gen strain were included in the experiment.

Overview of transcriptome responses to smoltification and SWT

The gene expression changes were sizeable in terms of both number of genes and magnitude already at smoltification and further augmented in all tissues one week after SWT (SWT1; Fig. 1). At SWT2, three weeks after SWT, an additional increase was observed in HK and gill while the number of regulated genes and the magnitude of differential expression were reduced in the intestine. During smoltification the transcriptome changes were smallest in the gill and relatively equal in the head kidney and

Discussion

Even though parr-smolt transformation is one of the most important and active research areas of salmon biology, surprisingly little attention is given to the complex interrelationships between hormonal changes and the immune system in today's Atlantic salmon aquaculture practices. Changes in immune competence can be anticipated considering the high energy costs associated with endocrine stimulation and metabolic and developmental processes, which are compared with metamorphosis by magnitude.

Acknowledgements

Study was supported with a grant from The Norwegian Seafood Research Fund – FHF “Multifactorial diseases in Norwegian Atlantic salmon farming” (900658). We thank Kari Steiro for technical assistance in the laboratory.

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