Gill Transcriptomic Responses to Toxin-producing Alga Prymnesium parvum in Rainbow Trout.

Morag Clinton,Niels Lorenzen,Per Juel Hansen,Dagoberto Sepúlveda,Samuel A M Martin,Nikolaj R Andersen,David E K Ferrier,Elżbieta Król,Andrew S Brierley

doi:10.3389/fimmu.2021.794593

Abstract

The gill of teleost fish is a multifunctional organ involved in many physiological processes, including protection of the mucosal gill surface against pathogens and other environmental antigens by the gill-associated lymphoid tissue (GIALT). Climate change associated phenomena, such as increasing frequency and magnitude of harmful algal blooms (HABs) put extra strain on gill function, contributing to enhanced fish mortality and fish kills. However, the molecular basis of the HAB-induced gill injury remains largely unknown due to the lack of high-throughput transcriptomic studies performed on teleost fish in laboratory conditions. We used juvenile rainbow trout (Oncorhynchus mykiss) to investigate the transcriptomic responses of the gill tissue to two (high and low) sublethal densities of the toxin-producing alga Prymnesium parvum, in relation to non-exposed control fish. The exposure time to P. parvum (4–5 h) was sufficient to identify three different phenotypic responses among the exposed fish, enabling us to focus on the common gill transcriptomic responses to P. parvum that were independent of dose and phenotype. The inspection of common differentially expressed genes (DEGs), canonical pathways, upstream regulators and downstream effects pointed towards P. parvum-induced inflammatory response and gill inflammation driven by alterations of Acute Phase Response Signalling, IL-6 Signalling, IL-10 Signalling, Role of PKR in Interferon Induction and Antiviral Response, IL-8 Signalling and IL-17 Signalling pathways. While we could not determine if the inferred gill inflammation was progressing or resolving, our study clearly suggests that P. parvum blooms may contribute to the serious gill disorders in fish. By providing insights into the gill transcriptomic responses to toxin-producing P. parvum in teleost fish, our research opens new avenues for investigating how to monitor and mitigate toxicity of HABs before they become lethal.

Highlights

The gill of teleost fish is a complex organ whose function goes beyond extracting oxygen from water and excreting carbon dioxide
The principal component analysis (PCA) of the gill transcriptome profiles in rainbow trout from high response (HH), high exposure/ moderate response (HM), low exposure/low response (LL) and C groups demonstrated a partial overlap between groups of fish exposed to P. parvum (HH, HM and LL) and their clear separation from the non-exposed control group (C) (Figure 1)
Based on the three sets of differentially expressed genes (DEGs) with 1436, 1069 and 567 transcripts, IPA identified 34, 95 and 33 canonical pathways that were significantly altered in the gill transcriptome of fish from HH, HM and LL groups, respectively, at B-H p-value < 0.001 (Supplementary Tables 5–7)

Summary

Introduction

The gill of teleost fish is a complex organ whose function goes beyond extracting oxygen from water and excreting carbon dioxide. Apart from the respiratory gas exchange, the gill plays a key role in osmotic and ionic regulation, acid-base balance, and excretion of nitrogenous waste [1] Because these processes are predominantly surface-dependent, the gill tissue consists of a highly complex system of branching vascular structures (primary and secondary lamellae) that are separated from the environment only by a thin layer of gill epithelium and mucosa [2, 3]. But not least, the gill surface provides major ports of entry for pathogens (via transepithelial transport) or site of interaction with other harmful invertebrates, such as water-born parasites and cnidarian jellyfish [10] To meet these challenges, the gill is strategically equipped with its own immune system, called the gill-associated lymphoid tissue (GIALT), thereby substantially contributing to overall fish health and survival [2, 3]. The GIALT consists of a panel of resident immune cells, including B and T cells, monocytes, macrophages, neutrophils, thrombocytes, dendritic-like cells, natural killer-like cells, eosinophilic granule cells, rodlet cells, and melanin-containing cells among the others [11, 12]

Methods

Results

Conclusion