Salmon louse labial gland enzymes: implications for host settlement and immune modulation

Helena Marie Doherty Midtbø; Christiane Eichner; Lars Are Hamre; Michael Dondrup; Linn Flesland; Kristoffer Helland Tysseland; Heidi Kongshaug; Andreas Borchel; Renate Hvidsten Skoge; Frank Nilsen; Aina-Cathrine Øvergård

doi:10.3389/fgene.2023.1303898

Salmon louse labial gland enzymes: implications for host settlement and immune modulation

Front Genet. 2024 Jan 17:14:1303898. doi: 10.3389/fgene.2023.1303898. eCollection 2023.

Affiliations

¹ Sea Lice Research Centre, Department of Biological Sciences, University of Bergen, Bergen, Norway.
² Sea Lice Research Centre, Department of Informatics, University of Bergen, Bergen, Norway.

Abstract

Salmon louse (Lepeophtheirus salmonis) is a skin- and blood-feeding ectoparasite, infesting salmonids. While feeding, labial gland proteins from the salmon louse may be deposited on the Atlantic salmon (Salmo salar) skin. Previously characterized labial gland proteins are involved in anti-coagulation and may contribute to inhibiting Atlantic salmon from mounting a sufficient immune response against the ectoparasite. As labial gland proteins seem to be important in the host-parasite interaction, we have, therefore, identified and characterized ten enzymes localized to the labial gland. They are a large group of astacins named L. salmonis labial gland astacin 1-8 (LsLGA 1-8), one serine protease named L. salmonis labial gland serine protease 1 (LsLGSP1), and one apyrase named L. salmonis labial gland apyrase 1 (LsLGAp1). Protein domain predictions showed that LsLGA proteins all have N-terminal ShK domains, which may bind to potassium channels targeting the astacins to its substrate. LsLGA1 and -4 are, in addition, expressed in another gland type, whose secrete also meets the host-parasite interface. This suggests that LsLGA proteins may have an anti-microbial function and may prevent secondary infections in the wounds. LsLGAp1 is predicted to hydrolyze ATP or AMP and is, thereby, suggested to have an immune dampening function. In a knockdown study targeting LsLGSP1, a significant increase in IL-8 and MMP13 at the skin infestation site was seen under LsLGSP1 knockdown salmon louse compared to the control, suggesting that LsLGSP1 may have an anti-inflammatory effect. Moreover, most of the identified labial gland proteins are expressed in mature copepodids prior to host settlement, are not regulated by starvation, and are expressed at similar or higher levels in lice infesting the salmon louse-resistant pink salmon (Oncorhynchus gorbuscha). This study, thereby, emphasizes the importance of labial gland proteins for host settlement and their immune dampening function. This work can further contribute to anti-salmon louse treatment such as vaccine development, functional feed, or gene-edited salmon louse-resistant Atlantic salmon.

Keywords: 5-nucleotidase; RNA interference; arthropod; copepod; development; gene expression; transcriptomics; trypsin.

Grants and funding

The authors declare that financial support was received for the research, authorship, and/or publication of this article. This research was funded by the Research Council Norway, SFI-Sea Lice Research Centre (grant number 203513/O30), the Norwegian Seafood Research Fund (FHF) (grant number 901564), and the European Union Horizon 2020 project ParaFishControl (grant number 634429). The Genomics Core Facility (GCF) at the University of Bergen, which is a part of the NorSeq consortium, provided services on RNA sequencing; the GCF was supported in part by major grants from the Research Council of Norway (grant number 245979/F50) and Bergen Research Foundation (BFS) (grant numbers BFS2017TMT04 and BFS2017TMT08).