AUTHOR=Emam Mohamed , Caballero-Solares Albert , Xue Xi , Umasuthan Navaneethaiyer , Milligan Barry , Taylor Richard G. , Balder Rachel , Rise Matthew L. 

TITLE=Gill and Liver Transcript Expression Changes Associated With Gill Damage in Atlantic Salmon (Salmo salar)

JOURNAL=Frontiers in Immunology

VOLUME=13

YEAR=2022

URL=https://www.frontiersin.org/journals/immunology/articles/10.3389/fimmu.2022.806484

DOI=10.3389/fimmu.2022.806484

ISSN=1664-3224

ABSTRACT=<p>Gill damage represents a significant challenge in the teleost fish aquaculture industry globally, due to the gill’s involvement in several vital functions and direct contact with the surrounding environment. To examine the local and systemic effects accompanying gill damage (which is likely to negatively affect gill function) of Atlantic salmon, we performed a field sampling to collect gill and liver tissue after several environmental insults (e.g., harmful algal blooms). Before sampling, gills were visually inspected and gill damage was scored; gill scores were assigned from pristine [gill score 0 (GS0)] to severely damaged gills (GS3). Using a 44K salmonid microarray platform, we aimed to compare the transcriptomes of pristine and moderately damaged (i.e., GS2) gill tissue. Rank Products analysis (5% percentage of false-positives) identified 254 and 34 upregulated and downregulated probes, respectively, in GS2 compared with GS0. Differentially expressed probes represented genes associated with functions including gill remodeling, wound healing, and stress and immune responses. We performed gill and liver qPCR for all four gill damage scores using microarray-identified and other damage-associated biomarker genes. Transcripts related to wound healing (e.g., <italic>neb</italic> and <italic>klhl41b</italic>) were significantly upregulated in GS2 compared with GS0 in the gills. Also, transcripts associated with immune and stress-relevant pathways were dysregulated (e.g., downregulation of <italic>snaclec 1-like</italic> and upregulation of <italic>igkv3</italic>) in GS2 compared with GS0 gills. The livers of salmon with moderate gill damage (i.e., GS2) showed significant upregulation of transcripts related to wound healing (i.e., <italic>chtop</italic>), apoptosis (e.g., <italic>bnip3l</italic>), blood coagulation (e.g., <italic>f2</italic> and <italic>serpind1b</italic>), transcription regulation (i.e., <italic>pparg</italic>), and stress-responses (e.g., <italic>cyp3a27</italic>) compared with livers of GS0 fish. We performed principal component analysis (PCA) using transcript levels for gill and liver separately. The gill PCA showed that PC1 significantly separated GS2 from all other gill scores. The genes contributing most to this separation were <italic>pgam2</italic>, <italic>des</italic>, <italic>neb</italic>, <italic>tnnt2</italic>, and <italic>myom1.</italic> The liver PCA showed that PC1 significantly separated GS2 from GS0; levels of <italic>hsp70</italic>, <italic>cyp3a27</italic>, <italic>pparg</italic>, <italic>chtop</italic>, and <italic>serpind1b</italic> were the highest contributors to this separation. Also, hepatic acute phase biomarkers (e.g., <italic>serpind1b</italic> and <italic>f2</italic>) were positively correlated to each other and to gill damage. Gill damage-responsive biomarker genes and associated qPCR assays arising from this study will be valuable in future research aimed at developing therapeutic diets to improve farmed salmon welfare.</p>