Interplay between a bacterial pathogen and its host in rainbow trout isogenic lines with contrasted susceptibility to cold water disease

Lee, Bo-Hyung; Quillet, Edwige; Rigaudeau, Dimitri; Dechamp, Nicolas; Duchaud, Éric; Bernardet, Jean‐François; Boudinot, Pierre; Rochat, Tatiana

doi:10.1016/j.micinf.2023.105140

Cited by 4 publications

(4 citation statements)

References 52 publications

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“…The ARS-Fp-S line fish exhibited a greater number of regulated genes, and expression levels were positively correlated with Fp load (27). This pattern is also observed between clonal lines of resistant and susceptible rainbow trout (31,40). Regulated genes included interleukins, tumor necrosis factor (TNF) receptor superfamily members, chemokines, complement components, acute phase response genes, nod-like receptor family members, and genes putatively involved in metabolism and wound healing.…”

Section: Introductionmentioning

confidence: 78%

“…Recently, Ali and Salem (86) report the identification and differential expression of several long-noncoding natural antisense transcripts complementary to hemolysis-related genes on day 5 post-infection, in the same populations of fish used in this study, suggesting enhanced clearance of free hemoglobin and heme and possibly increased erythropoiesis. In summary, blood and muscle components are released into the plasma, enhancing bacterial growth in tissues and blood (40), and it is possible that these host components may also act as endogenous damage-associated molecular patterns driving NLRP-mediated inflammation (87,88). Recently, Liu et al ( 89) identified nlrp1 on Chr8 as a candidate gene involved in genetic resistance.…”

Section: Pathophysiology Of Infection and Tissue Damagementioning

confidence: 99%

“…TCBP1 overexpression in the HEK-293 cells increased the active form of NF-kB and resulted in cell death, suggesting a proapoptotic function (99). Recently, a c1qtnf4 gene was upregulated 3 days post-infection in a clonal line of rainbow trout exhibiting high susceptibility to BCWD but was not regulated in two other lines with either intermediate or higher relative resistance (40). The protein encoded by the c1qtnf4 gene, XP_021456913.1, was not identified in plasma in our study.…”

Section: A Novel Biomarker Plasma C1q-lp3 Was Elevated In the Suscept...mentioning

confidence: 99%

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Plasma proteomic profiling of bacterial cold water disease-resistant and -susceptible rainbow trout lines and biomarker discovery

Wiens,

Marancik,

Chadwick

et al. 2023

Front. Immunol.

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Genetic variation for disease resistance is present in salmonid fish; however, the molecular basis is poorly understood, and biomarkers of disease susceptibility/resistance are unavailable. Previously, we selected a line of rainbow trout for high survival following standardized challenge with Flavobacterium psychrophilum (Fp), the causative agent of bacterial cold water disease. The resistant line (ARS-Fp-R) exhibits over 60 percentage points higher survival compared to a reference susceptible line (ARS-Fp-S). To gain insight into the differential host response between genetic lines, we compared the plasma proteomes from day 6 after intramuscular challenge. Pooled plasma from unhandled, PBS-injected, and Fp-injected groups were simultaneously analyzed using a TMT 6-plex label, and the relative abundance of 513 proteins was determined. Data are available via ProteomeXchange, with identifier PXD041308, and the relative protein abundance values were compared to mRNA measured from a prior, whole-body RNA-seq dataset. Our results identified a subset of differentially abundant intracellular proteins was identified, including troponin and myosin, which were not transcriptionally regulated, suggesting that these proteins were released into plasma following pathogen-induced tissue damage. A separate subset of high-abundance, secreted proteins were transcriptionally regulated in infected fish. The highest differentially expressed protein was a C1q family member (designated complement C1q-like protein 3; C1q-LP3) that was upregulated over 20-fold in the infected susceptible line while only modestly upregulated, 1.8-fold, in the infected resistant line. Validation of biomarkers was performed using immunoassays and C1q-LP3, skeletal muscle troponin C, cathelcidin 2, haptoglobin, leptin, and growth and differentiation factor 15 exhibited elevated concentration in susceptible line plasma. Complement factor H-like 1 exhibited higher abundance in the resistant line compared to the susceptible line in both control and challenged fish and thus was a baseline differentiator between lines. C1q-LP3 and STNC were elevated in Atlantic salmon plasma following experimental challenge with Fp. In summary, these findings further the understanding of the differential host response to Fp and identifies salmonid biomarkers that may have use for genetic line evaluation and on-farm health monitoring.

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Section: Introductionmentioning

confidence: 78%

Section: Pathophysiology Of Infection and Tissue Damagementioning

confidence: 99%

Section: A Novel Biomarker Plasma C1q-lp3 Was Elevated In the Suscept...mentioning

confidence: 99%

See 1 more Smart Citation

Plasma proteomic profiling of bacterial cold water disease-resistant and -susceptible rainbow trout lines and biomarker discovery

Wiens,

Marancik,

Chadwick

et al. 2023

Front. Immunol.

View full text Add to dashboard Cite

show abstract

“…Isolates sampling is biased toward fish farms and only few publications mentioned F. psychrophilum in natural fish populations [ 14 , 33 ]. Intrinsic host resistance/susceptibility should also be considered and the use of rainbow trout isogenic lines or full-sib families has revealed considerable differences inside a single host species [ 34 , 35 ].…”

Section: Discussionmentioning

confidence: 99%

Host specificity and virulence of Flavobacterium psychrophilum: a comparative study in ayu (Plecoglossus altivelis) and rainbow trout (Oncorhynchus mykiss) hosts

Fujiwara-Nagata,

Rochat,

Lee

et al. 2024

Vet Res

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Flavobacterium psychrophilum, the causative agent of bacterial cold-water disease, is a devastating, worldwide distributed, fish pathogen causing significant economic loss in inland fish farms. Previous epidemiological studies showed that prevalent clonal complexes (CC) differ in fish species affected with disease such as rainbow trout, coho salmon and ayu, indicating significant associations between particular F. psychrophilum genotypes and host species. Yet, whether the population structure is driven by the trade of fish and eggs or by host-specific pathogenicity is uncertain. Notably, all F. psychrophilum isolates retrieved from ayu belong to Type-3 O antigen (O-Ag) whereas only very few strains retrieved from other fish species possess this O-Ag, suggesting a role in outbreaks affecting ayu. Thus, we investigated the links between genotype and pathogenicity by conducting comparative bath infection challenges in two fish hosts, ayu and rainbow trout, for a collection of isolates representing different MLST genotypes and O-Ag. Highly virulent strains in one host species exhibited low to no virulence in the other. F. psychrophilum strains associated with ayu and possessing Type-3 O-Ag demonstrated significant variability in pathogenicity in ayu, ranging from avirulent to highly virulent. Strikingly, F. psychrophilum strains retrieved from rainbow trout and possessing the Type-3 O-Ag were virulent for rainbow trout but not for ayu, indicating that Type-3 O-Ag alone is not sufficient for pathogenicity in ayu, nor does it prevent pathogenicity in rainbow trout. This study revealed that the association between a particular CC and host species partly depends on the pathogen’s adaptation to specific host species.

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Systemic immune response of rainbow trout exposed to Flavobacterium psychrophilum infection

Deng,

Wang,

et al. 2024

Fish & Shellfish Immunology

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Interplay between a bacterial pathogen and its host in rainbow trout isogenic lines with contrasted susceptibility to cold water disease

Cited by 4 publications

References 52 publications

Plasma proteomic profiling of bacterial cold water disease-resistant and -susceptible rainbow trout lines and biomarker discovery

Plasma proteomic profiling of bacterial cold water disease-resistant and -susceptible rainbow trout lines and biomarker discovery

Host specificity and virulence of Flavobacterium psychrophilum: a comparative study in ayu (Plecoglossus altivelis) and rainbow trout (Oncorhynchus mykiss) hosts

Systemic immune response of rainbow trout exposed to Flavobacterium psychrophilum infection

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