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Flavobacterium Columnare Associated with Mortality of Salmonids Farmed in Chile: a Case Report of Two Outbreaks

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Flavobacterium Columnare Associated with Mortality of Salmonids Farmed in Chile: a Case Report of Two Outbreaks Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 36 NOTE Flavobacterium columnare associated with mortality of salmonids farmed in Chile: a case report of two outbreaks R. Avendaño-Herrera1*, V. Gherardelli2, P. Olmos2, M. G. Godoy2, A. Heisinger3 and J. Fernández4 1 Universidad Andrés Bello, Facultad de Ciencias Básicas, Departamento de Ciencias Básica. Viña del Mar, Chile;2 Laboratorio Aquagestion, Puerto Mon, Chile;3Multiexport Foods, Puerto Mon, Chile;4 Instituto de Salud Pública, Santiago Abstract Since 2007 when infectious salmon anaemia virus was reported in Atlantic salmon (Salmo salar), the Chilean aquaculture industry has been restructured and intensification of Pacific salmon (Oncorhynchus kisutch) and rainbow trout (Oncorhynchus mykiss) farming has resulted in growing problems of emergent freshwater pathogens. This work reports the isolation, identification and characterization of a group of Chilean Flavobacterium columnare isolates from recent episodes of outbreaks in Pacific salmon and rainbow trout farms in Rupanco Lake in Chile. Flavobacterium columnare is the etiological agent at least 36 species of fish in several geographical of columnaris disease, one of the most predomi- areas have been identified as susceptible to F. nant bacterial diseases of freshwater fish. This columnare (Shoemaker et al., 2003). Columnaris Gram-negative bacterium infects wild, farmed disease generally causes characteristic white to and ornamental fish species worldwide and yellow erosion in the tegument, severe necrosis oVen causes remarkable financial and mate- of the gill and skin epithelium, and in some rial losses yearly for the fish farming industry instances it also can be isolated from moribund (Bader and Starliper, 2002; Wagner et al., 2002). fish, exhibiting lile or no gross clinical signs of In fact, infections are the second leading cause infection (Decostere et al., 1998; Olivares-Fuster of mortality in pond raised channel catfish (Ic- et al., 2007). talurus punctatus) in the south-eastern United States (Wagner et al., 2002; Durborrow et al., AVer Norway, Chile was the second major 1988). salmon producer during several years, espe- cially Atlantic salmon (Salmo salar), with an The species was first described by Davis (1922) in estimated production of approximately 400000 numerous freshwater fishes, and subsequently ton during 2007 (hp://www.salmonchile.cl), * Corresponding author’s email: [email protected] or [email protected] Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 37 surprisingly no cases of columnaris disease were The mortality rate in Farm A was lower than noted in Chilean aquaculture. However, aVer the Farm B, but continuous during the course of the outbreaks of infectious salmon anaemia virus in outbreak (one month). The distance between the marine farmed Atlantic salmon in June of 2007 two farms is approximately 4 km. Both farms (Godoy et al., 2008), the Chilean aquaculture were using water from the Rupanco Lake in industry has restructured itself and currently is their fish cultures. The origin of all fish was showing an increased interest in the cultivation from eggs spawned in Chile. The affected fish of Pacific salmon (Oncorhynchus kisutch) and were farmed at a water temperature of 16 ± 1ºC rainbow trout (Oncorhynchus mykiss). When during the different outbreaks. compared to February 2009, current exports of rainbow trout have increased 36% (www. A total of 5 moribund fish from each disease ifop.cl). outbreak was transported to the laboratory facilities in plastic bags for pathological and The intensification of fish farming in freshwater bacteriology examination. Scrapings obtained environments has resulted in the emergence of from gills and skin lesions were used for micro- freshwater bacterial pathogens such as atypical scopic observation and microbiological analysis. Aeromonas salmonicida (Godoy et al., 2010) and Ten slides (equivalent of 2 different samples more recently F. columnare. In this study, we per fish) were also stained using Gram stain. report recent outbreaks of columnaris disease Moribund fish were euthanized by an overdose in Pacific salmon and rainbow trout farms in a of benzocaine and subjected to post-mortem ex- freshwater lake in Chile and describe, for the amination. Internal analysis showed pale liver, first time, the characterization of F. columnare splenomegalia, swollen kidney that contained associated with mortality. white nodules, ascitis and enteritis. Samples from gills and kidney were streaked onto TYES In February 2010 mortalities occurred in young agar plates (tryptone yeast extract salts medium: rainbow trout (25–35 g) at a rearing site (Farm 0.4% tryptone, 0.05% yeast extract, 0.02% an- A) in Rupanco Lake located 112 km at north- hydrous calcium chloride, 0.05% magnesium west Osorno (X Región) of Chile. The external sulphate heptahydrate, pH 7.2) and incubated gross finding noted in affected fish included aerobically at 15ºC for up to 10 days. eroded fins and tail rot and pale gills with ac- cumulations of mucus of yellow color on the Microscopic examinations of wet mount and filaments. Gram stained smears from gills lesions of both fish species revealed the presence of many long Twenty five days later, another outbreak oc- rods, thin with the ability to flex. Yellow pig- curred in smolt of Pacific salmon in the same mented colonies inoculated from gill lesions area, but in another farm (Farm B). The size of of all rainbow trout samples grew on all the the affected fish ranged from 60 to 70 g and the TYES plates and were observed aVer 4 to 6 pathology observed was similar to the described days post-incubation. Pure cultures of yellow for rainbow trout. colonies were also obtained from both rainbow trout and Pacific salmon kidney samples. Three Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 38 yellow-pigmented bacterial isolates were taken tochrome oxidase and catalase tests. Colonies for identification using biochemical and genetic were flat with rhizoid edges and strongly adher- studies. The isolates LM-01-Fc and LM-03-Fc ent to the medium and color shiVed from yellow were recovered from rainbow trout gills and to pink in presence of 3% sodium hydroxide. All kidney, respectively, while the isolate LM-02- isolates contained a cell-wall-associated flexiru- Fc was obtained from Pacific salmon kidney. bin-type pigment (KOH method according to Then, total genomic DNA was extracted from Reichenbach, 1989), absorbed Congo red and each isolate in pure colonies using InstaGeneTM produced diffusible gelatin degrading enzyme. Matrix (Bio-Rad) according to the manufacturer Chondroitinase activity from the culture su- instructions. All DNAs were maintained at – pernatant of the three isolates (Stringer-Roth 20ºC until they were used for PCR reactions. et al., 2002) was detected only in the Pacific Stock cultures were maintained frozen at –80ºC salmon isolate. Interestingly, the production of in Criobilles tubes (AES Laboratories). chondroitinase has been related to the virulence of F. columnare due to it causes necrotic lesions Initially, the recovered isolates were presump- by degrading chondroitin in the extracellular tively diagnosed as members of the F. psy- matrix of the fish tissue (Stringer-Roth et al., chrophilum species. However, the three strains 2002; Suomalainen et al., 2006). were not recognized by the Urdaci et al., (1998) and Izumi et al., (2003) pair of primers, indicat- Other phenotypic features of these isolates were ing that the pigmented isolates were distinct performed using API ZYM (bioMérieux) strips, from F. psychrophilum. These and all other PCR according to the manufacturer’s instruction with assays described in this work were performed the exception of the incubation temperature, following the protocol described by each author which was fixed at 25°C. The type strain F. co- with the exception that PCR reactions were lumnare ATCC 23462T from the American Type carried out using the commercial kit PuReTaqTM Culture Collection was included for compara- Ready-To-GoTM PCR beads (GE Healthcare), tive purpose. The presence and activity of 19 which included all the reagents needed for enzymes in the API ZYM gallery showed that the PCR reactions (buffer, nucleotides and Taq all isolates were similar in number of detected DNA polymerase), with the exception of the enzymes and level of enzymatic activity pro- specific primers and DNA template. The reac- duced, i.e. the typical profile of the F. columnare tion mixtures were amplified in a Mastercycler reference strain. personal (Eppendorf) apparatus. As for the PCR assays, similar finding was observed when In particular, none of the enzymes involved bacterial colonies were tentatively identified in the metabolism of carbohydrates could be by an indirect fluorescent antibody tests (IFAT, detected, similar to the reports of Michel et al., BiosChile), confirming that all Chilean isolates (2002) and Austin and Austin (2007). were not F. psychrophilum. Antimicrobial tests were applied by disc diffu- Biochemically, the isolated bacteria were Gram- sion method on dilute versions of Mueller-Hin- negative, non-motile, and positive for the cy- ton medium as recommended by the Clinical Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 39 Laboratory Standards Institute (CLSI, 2006) for (CLSI, 2006). Despite the fact that the majority use with F. columnare and F. psychrophilum. The of the drugs tested were effective in vitro, fish reference strain A. salmonicida subsp. salmonicida mortality was reduced following oral treatments ATCC 33658 was grown on Mueller–Hinton with florfenicol (15 mg kg-1 fish for 15 days). agar and used as control. All Chilean strains presented an identical antimicrobial suscep- Based on the phenotypic and biochemical char- tibility paern. They were highly susceptible acteristics, the bacteria recovered from necrop- to amoxicillin (AMX, 25 μg), enrofloxacine sied fish were consistent with characteristics of (ENR, 5 μg), florfenicol (FFC, 30 μg) and ox- F. columnare. To confirm this observation, the ytetracycline (OT, 30 μg) with mean inhibition specific PCR-analysis described by Welker et al., zones sizes ranging from 50 to 60 mm, while (2005) to identify the intergenic spacer region the oxolinic acid (AO, 2 μg) and trimethoprim- (ISR) between 16S–23S rRNA of F.
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