Integration of Transcriptome, Gross Morphology and Histopathology in the Gill of Sea Farmed Atlantic Salmon (Salmo salar): Lessons From Multi-Site Sampling.

Elżbieta Król,Patricia Noguera,Sophie Shaw,Alex Douglas,Eoin Costelloe,Karina Gajardo,Ralph Bickerdike,Samuel A M Martin,Victoria Valdenegro

doi:10.3389/fgene.2020.00610

Elżbieta Król, Patricia Noguera + Show 7 more

Open Access

https://doi.org/10.3389/fgene.2020.00610

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Abstract

The gill of teleost fish is a multifunctional organ involved in many physiological processes such as gas exchange, osmotic and ionic regulation, acid-base balance and excretion of nitrogenous waste. Due to its extensive interface with the environment, the gill plays a key role as a primary mucosal defense tissue against pathogens, as manifested by the presence of the gill-associated lymphoid tissue (GIALT). In recent years, the prevalence of multifactorial gill pathologies has increased significantly, causing substantial losses in Atlantic salmon aquaculture. The transition from healthy to unhealthy gill phenotypes and the progression of multifactorial gill pathologies, such as proliferative gill disease (PGD), proliferative gill inflammation (PGI) and complex gill disorder (CGD), are commonly characterized by epithelial hyperplasia, lamellar fusion and inflammation. Routine monitoring for PGD relies on visual inspection and non-invasive scoring of the gill tissue (gross morphology), coupled with histopathological examination of gill sections. To explore the underlying molecular events that are associated with the progression of PGD, we sampled Atlantic salmon from three different marine production sites in Scotland and examined the gill tissue at three different levels of organization: gross morphology with the use of PGD scores (macroscopic examination), whole transcriptome (gene expression by RNA-seq) and histopathology (microscopic examination). Our results strongly suggested that the changes in PGD scores of the gill tissue were not associated with the changes in gene expression or histopathology. In contrast, integration of the gill RNA-seq data with the gill histopathology enabled us to identify common gene expression patterns associated with multifactorial gill disease, independently from the origin of samples. We demonstrated that the gene expression patterns associated with multifactorial gill disease were dominated by two processes: a range of immune responses driven by pro-inflammatory cytokines and the events associated with tissue damage and repair, driven by caspases and angiogenin.

Highlights

The gill of teleost fish is a multifunctional organ involved in many physiological processes such as gas exchange, osmotic and ionic regulation, acid-base balance and excretion of nitrogenous waste (Evans et al, 2005)
By sampling sea farmed Atlantic salmon at three production sites (A, B and C) in Scotland, we demonstrated that the gill samples from different sites had different histopathology (Figure 4B) and different transcriptomic profiles (Figure 3B), with 240 to 1360 genes identified as differentially expressed between the sites (Table 4)
Recent increases in gill pathologies in sea farmed Atlantic salmon highlight the need to establish the molecular basis of multifactorial gill disease to improve diagnosis and preventive measures of this condition

Summary

Introduction

The gill of teleost fish is a multifunctional organ involved in many physiological processes such as gas exchange, osmotic and ionic regulation, acid-base balance and excretion of nitrogenous waste (Evans et al, 2005) To facilitate these functions, the gill tissue has evolved into a highly complex system of branching vascular structures (lamellae), separated from the external milieu only by a thin layer of gill epithelium and mucosa (Koppang et al, 2015; Salinas, 2015). The densely packed lamellar structure of the gill is highly advantageous because it provides a large surface area for oxygen transfer, amounting to approximately 0.1–0.4 m2 of lamellar surface per kg of body mass (Maina, 2011; Park et al, 2014) Having such an extensive interface with the environment comes at a high price (reviewed in Nilsson, 2007). To combat pathogens and parasites, the gill is equipped with the gill-associated lymphoid tissue (GIALT), adding another dimension to the importance of this organ to fish functioning and survival (Koppang et al, 2015; Salinas, 2015; Xu et al, 2020)

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