Profiling the transcriptome response of Atlantic salmon head kidney to formalin-killed Renibacterium salmoninarum

Eslamloo, Khalil; Kumar, Surendra; Caballero‐Solares, Albert; Gnanagobal, Hajarooba; Santander, Javier; Rise, Matthew L.

doi:10.1016/j.fsi.2019.11.057

Cited by 27 publications

(44 citation statements)

References 76 publications

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“…A recent study reported expression responses of 22 genes (e.g., transcripts encoding interleukins and interferons) in the head kidney of Atlantic salmon infected with R. salmoninarum at different temperatures (16). Since vaccination with formalin-killed R. salmoninarum was found to enhance the resistance of salmonids to BKD (9), microarrays were previously used to profile the transcriptome response of Atlantic salmon to formalin-killed R. salmoninarum bacterin (17). Although this previous study enhanced our understanding of the Atlantic salmon immune response to R. salmoninarum-derived antigens, the transcriptome response and molecular pathways underlying Atlantic salmon response to live R. salmoninarum pathogen remained uncharacterised before the current study.…”

Section: Introductionmentioning

confidence: 99%

“…Microarray analyses can determine the transcriptome profile of immunological responses in a species (18). In addition to the aforementioned R. salmoninarum bacterin study (17), microarrays were previously employed to profile the antibacterial responses of Atlantic salmon to other bacterial pathogens such as Piscirickettsia salmonis (19), and Aeromonas salmonicida (20,21) as well as commercial vaccines (e.g., for immunisation against Yersinia ruckeri and Vibrio spp.) (22,23).…”

Section: Introductionmentioning

confidence: 99%

“…The consortium for Genomic Research on All Salmonids Project (cGRASP)-designed Agilent 44K salmonid oligonucleotide microarray (24) was previously used in several immune-related studies in Atlantic salmon and rainbow trout (17,(25)(26)(27)(28)(29). In the present study, we used this powerful microarray platform to identify Atlantic salmon head kidney transcripts responsive to R. salmoninarum pathogen and determine if the level of R. salmoninarum infection [i.e., higher and lower susceptibility levels corresponding to higher and lower infection levels, respectively, at 13 days post-infection/injection (dpi) as determined by TaqMan assays] influenced the Atlantic salmon response to BKD.…”

Section: Introductionmentioning

confidence: 99%

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Transcriptomic Profiling of the Adaptive and Innate Immune Responses of Atlantic Salmon to Renibacterium salmoninarum Infection

et al. 2020

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Bacterial Kidney Disease (BKD), which is caused by a Gram-positive, intracellular bacterial pathogen (Renibacterium salmoninarum), affects salmonids including Atlantic salmon (Salmo salar). However, the transcriptome response of Atlantic salmon to BKD remained unknown before the current study. We used a 44K salmonid microarray platform to characterise the global gene expression response of Atlantic salmon to BKD. Fish (∼54 g) were injected with a dose of R. salmoninarum (H-2 strain, 2 × 10 8 CFU per fish) or sterile medium (control), and then head kidney samples were collected at 13 days post-infection/injection (dpi). Firstly, infection levels of individuals were determined through quantifying the R. salmoninarum level by RNA-based TaqMan qPCR assays. Thereafter, based on the qPCR results for infection level, fish (n = 5) that showed no (control), higher (H-BKD), or lower (L-BKD) infection level at 13 dpi were subjected to microarray analyses. We identified 6,766 and 7,729 differentially expressed probes in the H-BKD and L-BKD groups, respectively. There were 357 probes responsive to the infection level (H-BKD vs. L-BKD). Several adaptive and innate immune processes were dysregulated in R. salmoninarum-infected Atlantic salmon. Adaptive immune pathways associated with lymphocyte differentiation and activation (e.g., lymphocyte chemotaxis, T-cell activation, and immunoglobulin secretion), as well as antigen-presenting cell functions, were shown to be differentially regulated in response to BKD. The infection level-responsive transcripts were related to several mechanisms such as the JAK-STAT signalling pathway, B-cell differentiation and interleukin-1 responses. Sixty-five microarray-identified transcripts were subjected to qPCR validation, and they showed the same fold-change direction as microarray results. The qPCRvalidated transcripts studied herein play putative roles in various immune processes including pathogen recognition (e.g., tlr5), antibacterial activity (e.g., hamp and camp), regulation of immune responses (e.g., tnfrsf11b and socs1), T-/B-cell differentiation (e.g., ccl4, irf1 and ccr5), T-cell functions (e.g., rnf144a, il13ra1b and tnfrsf6b), and Eslamloo et al. Atlantic Salmon Response to BKD antigen-presenting cell functions (e.g., fcgr1). The present study revealed diverse immune mechanisms dysregulated by R. salmoninarum in Atlantic salmon, and enhanced the current understanding of Atlantic salmon response to BKD. The identified biomarker genes can be used for future studies on improving the resistance of Atlantic salmon to BKD.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Transcriptomic Profiling of the Adaptive and Innate Immune Responses of Atlantic Salmon to Renibacterium salmoninarum Infection

et al. 2020

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“…The present study addressed this gap of knowledge in the salmon's anti-parasitic immune response using a 44K consortium for Genomic Research on All Salmonids Project (cGRASP) microarray platform [27] which provides good coverage of the salmon transcriptome, together with real-time quantitative polymerase chain reaction (QPCR) for confirmation purposes. We have used this approach in our previous immune-relevant experiments for studying salmon immune transcriptome responses against viral mimic [28] and bacterial antigens [29]. We investigated the initial local host transcriptomic response in pelvic fin, the first dominant attachment sites of L. salmonis copepodids [30], of infected salmon by profiling the gene expression at attachment sites (ATT) and adjacent to chalimus-attachment sites (ADJ) compared to non-infected controls (PRE).…”

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confidence: 99%

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

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Caballero‐Solares

et al. 2020

IJMS

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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.

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“…Over time, several attempts have been made at developing bacterin-killed vaccines against BKD, for example, by heat inactivation of the bacterium. Formalin-killed bacterin have been shown to stimulate the expression of immune and immunoregulatory genes, including tlr5 and clec12b as well as tnfrsf6b and tnfrsf11b [ 109 ]. Similarly, specific immunogenic surface proteins have been identified in R. salmoninarum such as the major soluble antigen (MSA) [ 59 ], suggesting that it should be possible to develop a vaccine against this pathogen.…”

Section: Treatment Control and Disinfection Equipment Of mentioning

confidence: 99%

Renibacterium salmoninarum—The Causative Agent of Bacterial Kidney Disease in Salmonid Fish

2020

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Renibacterium salmoninarum is one of the oldest known bacterial pathogens of fish. This Gram-positive bacterium is the causative agent of bacterial kidney disease, a chronic infection that is mostly known to infect salmonid fish at low temperatures. Externally, infected fish can display exophthalmia as well as blebs on the skin and ulcerations alongside haemorrhages at the base of the fins and alongside the lateral line. Internally, the kidney, heart, spleen and liver can show signs of swelling. Granulomas can be seen on various internal organs, as can haemorrhages, and the organs can be covered with a false membrane. Ascites can also accumulate in the abdominal cavity. The bacterium is generally cultivated on specialized media such as kidney disease medium-1 (KDM-1), KDM-2 and selective kidney disease medium (SKDM), and a diagnostic is performed using molecular tools such as PCRs or real-time quantitative PCRs (RT-qPCRs). Several virulence mechanisms have been identified in R. salmoninarum, in particular the protein p57 that is known to play a role in both agglutination and immunosuppression of the host’s defense mechanisms. Control of the disease is difficult; the presence of asymptomatic carriers complicates the eradication of the disease, as does the ability of the bacterium to gain entrance inside the eggs. Bacterin-killed vaccines have proven to be of doubtful efficacy in controlling the disease, and even more recent application of a virulent environmental relative of R. salmoninarum is of limited efficacy. Treatment by antibiotics such as erythromycin, azithromycin and enrofloxacin can be effective but it is slow and requires prolonged treatment. Moreover, antibiotic-resistant strains have been reported. Despite being known for a long time, there is still much to be discovered about R. salmoninarum, notably regarding its virulence mechanisms and its vaccine potential. Consequently, these gaps in knowledge continue to hinder control of this bacterial disease in aquaculture settings.

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Profiling the transcriptome response of Atlantic salmon head kidney to formalin-killed Renibacterium salmoninarum

Cited by 27 publications

References 76 publications

Transcriptomic Profiling of the Adaptive and Innate Immune Responses of Atlantic Salmon to Renibacterium salmoninarum Infection

Transcriptomic Profiling of the Adaptive and Innate Immune Responses of Atlantic Salmon to Renibacterium salmoninarum Infection

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

Renibacterium salmoninarum—The Causative Agent of Bacterial Kidney Disease in Salmonid Fish

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