Transcriptomic Profiling in Fins of Atlantic Salmon Parasitized with Sea Lice: Evidence for an Early Imbalance Between Chalimus-Induced Immunomodulation and the Host's Defense Response.

Navaneethaiyer Umasuthan,Jillian D Westcott,Mark D Fast,Stanko Skugor,Xi Xue,Zhiyu Chen,Albert Caballero-Solares,Richard G Taylor,Matthew L Rise,Surendra Kumar,Barbara F Nowak

doi:10.3390/ijms21072417

Abstract

Parasitic sea lice (e.g., Lepeophtheirus salmonis) cause costly outbreaks in salmon farming. Molecular insights into parasite-induced host responses will provide the basis for improved management strategies. We investigated the early transcriptomic responses in pelvic fins of Atlantic salmon parasitized with chalimus I stage sea lice. Fin samples collected from non-infected (i.e., pre-infected) control (PRE) and at chalimus-attachment sites (ATT) and adjacent to chalimus-attachment sites (ADJ) from infected fish were used in profiling global gene expression using 44K microarrays. We identified 6568 differentially expressed probes (DEPs, FDR < 5%) that included 1928 shared DEPs between ATT and ADJ compared to PRE. The ATT versus ADJ comparison revealed 90 DEPs, all of which were upregulated in ATT samples. Gene ontology/pathway term network analyses revealed profound changes in physiological processes, including extracellular matrix (ECM) degradation, tissue repair/remodeling and wound healing, immunity and defense, chemotaxis and signaling, antiviral response, and redox homeostasis in infected fins. The QPCR analysis of 37 microarray-identified transcripts representing these functional themes served to confirm the microarray results with a significant positive correlation (p < 0.0001). Most immune/defense-relevant transcripts were downregulated in both ATT and ADJ sites compared to PRE, suggesting that chalimus exerts immunosuppressive effects in the salmon’s fins. The comparison between ATT and ADJ sites demonstrated the upregulation of a suite of immune-relevant transcripts, evidencing the salmon’s attempt to mount an anti-lice response. We hypothesize that an imbalance between immunomodulation caused by chalimus during the early phase of infection and weak defense response manifested by Atlantic salmon makes it a susceptible host for L. salmonis.

Highlights

Ectoparasitic arthropods are the most prominent aquatic pest threat to the fishery and fish-farming industries worldwide [1,2]
Pelvic fin tissue was sampled from non-infected fish (PRE; 0 days post-infection; n = 11), and salmon were experimentally infected with L. salmonis copepodids
The current study identified a total of 6568 non-redundant differentially expressed probes (DEPs) when three different groups were compared in pairs (i.e., 6227 in ADJ compared to PRE (ADJ versus PRE), 2239 in attachment sites (ATT) compared to PRE (ATT versus PRE), and 90 in ATT compared to ADJ (ATT versus ADJ)) at false discovery rate (FDR) < 5% (Figure 1A; Supplementary File S1)

Summary

Introduction

Ectoparasitic arthropods are the most prominent aquatic pest threat to the fishery and fish-farming industries worldwide [1,2]. Atlantic salmon (Salmo salar) is among the most intensively farmed finfish species [6,7], but is more vulnerable to L. salmonis infection [2,4] than some species of Pacific salmon (e.g., coho (O. kisutch) and pink (O. gorbuscha) salmon) [8,9]. This is thought to be primarily due to its weaker cellular response to the louse (i.e., the attached chalimus life stages), such as limited epithelial hyperplasia and inflammation [10], compared to other salmonids

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Conclusion