Antigens of the type-three secretion system of Aeromonas salmonicida subsp. salmonicida prevent protective immunity in rainbow trout

Abstract

Aeromonas salmonicida subsp. salmonicida is the etiologic agent of furunculosis, a frequent and significant disease of fisheries worldwide. The disease is largely controlled by commercial oil adjuvanted vaccines containing bacterins. However, the mechanisms leading to a protective immune response remain poorly understood. The type-three secretion system (T3SS) plays a central role in virulence of A. salmonicida subsp. salmonicida and thus may have an influence on the immune response of the host. The aim of this study was to evaluate the role of the T3SS antigens in mounting a protective immune response against furunculosis. Rainbow trout were intraperitoneally vaccinated in two independent experiments with bacterins prepared from a wild-type A. salmonicida strain and an isogenic strain carrying a deletion in the T3SS (ΔascV). Fish were challenged with the wt strain eight weeks after vaccination. In both trials, the survival rate of trout vaccinated with the ΔascV strain was significantly higher (23-28%) in comparison to the group vaccinated with the wt strain. High-throughput proteomics analysis of whole bacteria showed the ascV deletion in the mutant strain resulted in lower expression of all the components of the T3SS, several of which have a potential immunosuppressive activity. In a third experiment, fish were vaccinated with recombinant AcrV (homologous to the protective antigen LcrV of Yersinia) or S-layer protein VapA (control). AcrV vaccinated fish were not protected against a challenge while fish vaccinated with VapA were partially protected. The presence of T3SS proteins in the vaccine preparations decreased the level of protection against A. salmonicida infection and that AcrV was not a protective antigen. These results challenge the hypothesis that mounting specific antibodies against T3SS proteins should bring better protection to fish and demonstrate that further investigations are needed to better understand the mechanisms underlying effective immune responses against A. salmonicida infection.

Transcriptomic and proteomic analyses of splenic immune mechanisms of rainbow trout (Oncorhynchus mykiss) infected by Aeromonas salmonicida subsp. salmonicida

“…Over the years, a considerable number of studies have been conducted to reveal the immune mechanisms of rainbow trout against A. salmonicida at both physiological and molecular levels [8][9][10][11]. However, a lack of genomic data severely hampers further advancement in terms of revealing specific molecular targets.…”

Systemic infection in European perch with thermoadapted virulent Aeromonas salmonicida (Perca fluviatilis)

“…Furthermore, it had been shown that the type strain of A. salmonicida ATCC 7966T, which is avirulent, does not have a TTSS (Burr & Frey, 2009). TTSSs specify nanosyringes that allow the transfer of the corresponding effector proteins and toxins such as AexT from the cytosol of bacteria into the target host cells Vanden Bergh, Burr et al, 2013;. Some of these effector proteins have down-regulatory effects on phagocytosis, NF-κB signalling pathway and immune functions (Fast, Tse, Boyd, & Johnson, 2009;Fehr et al, 2006;Frey & Origgi, 2016;Origgi et al, 2017) and also infer with protective immunity of A. salmonicida vaccines against furunculosis (Vanden Bergh, Heller, Braga-Lagache, & Frey, 2013).…”

Characterization of Aeromonas salmonicida and A. sobria isolated from cultured salmonid fish in Korea and development of a vaccine against furunculosis

“…High pathogenic and mild pathogenic strains contained ascC and ascV genes in DNA and cDNA, while low pathogenic strain lacks ascC. Previous studies also demonstrated that low pathogenicity was resulted from a deficiency of T3SS apparatus genes (Bergh et al, 2013; Stuber, Burr, Braun, Wahli, & Frey, 2003). T3SS genes of A. salmonicida may be lost when cultured in stressful environments (Stuber et al, 2003), or may be rearranged by insertion sequence (IS) (Daher et al, 2011).…”

“…The major virulence factors identified in A. salmonicida are known as type three secretion system (T3SS) (Bergh et al, 2013; Daher et al, 2011; Frey & Origgi, 2016). T3SS is a protein accessory found in many negative bacteria that plays a key role in virulence and affects the host's immune response (Frey & Origgi, 2016).…”