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Cytophaga, Flavobacterium, Flexibacter and Chryseobacterium Infections in Cultured Marine Fish

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Cytophaga, Flavobacterium, Flexibacter and Chryseobacterium Infections in Cultured Marine Fish 魚 病 研 究 Fish Pathology,33(4),229-238,1998.10 Cytophaga, Flavobacterium, Flexibacter and Chryseobacterium Infections in Cultured Marine Fish J.-F.Bernardet Unite de Virologieet ImmunologieMoleculaires, Centre de Recherches INRA,78352 Jouy-en-Josascedex, France (Received February 2,1998) Many cases of fin or tail rot, skin ulcer, and jaw erosion were reported over the years in cultured marine fish. The aetiological role of various bacteria belonging to the Flavobacterium-Cytophaga group was frequently suspected, but only 3 bacterial species pathogenic for marine fish were fully described until now. Flexibacter maritimus was first identified in Japan in the late seventies from several fish species reared in sea water. Subsequently, the disease was recognized in very different geographic areas such as France, Scotland, Spain, Malta, Tasmania and California. The pathogenicity of the bacterium was demonstrated experimentally, phenotypic and genomic characteristics as well as virulence mechanisms were investigated, and treatment methods were proposed. Significant losses due to Flexibacter maritimus may occur locally. In Norway, Flexibacter ovolyticus was isolated from the adherent bacterial epiflora of Atlantic halibut eggs and was shown to be an opportunistic pathogen for halibut eggs and larvae. Chryseobacterium scophthalmum (first described under the epithet Flavobacterium scophthalmum) was isolated 10 years ago in Scotland from turbot suffering from gill hyperplasia and haemorrhagic septicaemia. A large collection of strains was studied, and investigations of the disease included experimental infection, histopa thology and immunization trials. Until now, Flexibacter ovolyticus and Chryseobacterium scophthalmum have not been recognized in fish species or regions other than those from which they were initially isolated. Key words : Cytophaga, Flexibacter, Flavobacterium,Chryseobacterium, marine fish Over the years, many authors have reported losses attempts for isolating these organisms were frequently among feral or cultured marine fish involving bacteria unsuccessfUl. Until now, only 3 bacterial species patho- belonging to the Flavobacterium-Cytophaga group. genic fbr marine fish have been isolated, fully described These conditions are worldwide and may be economi and named: Flexibacter maritimus (Wakabayashi et al., cally significant, locally. They have been described in 1986),Flexibacter ovolytic〃5(Hansen et al.,1992), and many different fish species, anadromous salmonids m scophthalmum(Mudarris et al., Chryseobacteriu raised in sea water as well as strictly marine species, cul 1994). tured in net-pens or concrete tanks (Devesa et al., 1989). In this review, recent taxonomic modifications con- Diseased fish usually exhibit severe necrotic lesions, ceming these bacteria will first be presented. Some such as fin and tail rot, skin ulcers, stomatitis or jaw examples of diseases in marine fish related to unidenti erosion, but septicaemiamay also occur. In many cases, fied bacteria belonging to this group will then be given, the aetiological role of Cytophaga-, Flexibacter-, or as well as more detailed informations about the 3 named Flavobacterium-like organisms was suspected because bacterial species. Lastly, the pathogenicity of some numerous long, slender, Gramnegative rods exhibiting Cytophaga-and Flexibacter-like organisms fbr molluscs gliding motility were observed in the lesions. However, and crustacea will be considered. Address for correspondence:Jean-FrangoisBernardet, Unit6 de Virologieet lmmunologie Mol6culaires, Centre de RecherchesINRA, Taxonomic background 78352 Jouy-en-Josascedex, France. Facsimilenumber:33134652591. E-mail address:jfb@biotec. Following extensivephylogenetic investigations jouy.inra.fr based on the study of rRNA sequence,menaquinone 230 J. F. Bernardet content, as well as fatty acid and whole-cell protein pro genus (i.e. S. myxococcoides) is a cellulolytic soil files (Nakagawa and Yamasato, 1993; Bernardet et al., organism (Reichenbach, 1989) phylogenetically related 1996), the taxonomy of the Flavobacterium-Bacteroides to the genus Cytophaga as recently emended (Bernardet phylum (also called rRNA superfamily V), to which the et al., 1996). Flavobacterium-Cytophaga group belongs, has gone through considerable modifications. Among other "Flavobacterium "-like organisms taxa, these modifications particularly concerned the Several bacteria phenotypically similar to members family Flavobacteriaceae (Bernardet et al., 1996) and of the genus Flavobacterium (as it was defined before related genera such as Cytophaga and Flexibacter. As the recent emendation restricted it to soil and freshwater a consequence of the very isolated position occupied by organisms) have been recognized from diseased marine the type species of these 2 genera within the superfam fish. From a yellowish slime on halibut skin, Harrison ily, the genus Cytophaga was restricted to 2 cellulolytic (1929) isolated Chryseobacterium (Flavobacterium) soil organisms (Nakagawa and Yamasato, 1996) and F. balustinum, but this bacterium has later been considered flexilis was considered the type and only species within a fish spoilage agent rather than a pathogen (Austin and the genus Flexibacter (Nakagawa and Yamasato, 1993; Austin, 1987). However, a very similar organism was Bernardet et al., 1996). Hence, all other bacterial later isolated from the heart blood of a dace (Leuciscus species previously included in these genera had to be leuciscus) exhibiting signs of haemorrhagic septicaemia reclassified. For instance, the freshwater fish patho in a French river (Brisou et al., 1959). As no strain gens Flexibacter (Cytophaga) columnaris, Flexibacter from halibut was preserved, the dace isolate became the (Cytophaga) psychrophilus, and Cytophaga johnsonae type strain of C. balustinum. All Chryseobacterium were allocated to the emended genus Flavobacterium, species being highly tolerant to salt (Bernardet, unpub together with Flavobacterium branchiophilum (Bernardet lished data), it is possible C. balustinum was isolated et al., 1996). The turbot pathogen Flavobacterium from both a marine and a freshwater fish. Very scophthalmum (Mudarris et al., 1994) was transferred recently, this bacterial species was also found in the to the new genus Chryseobacterium, together with intestines of healthy chum salmon (Oncorhynchus keta) several other nongliding organisms previously consid (Morita et al., 1997). ered Flavobacterium, such as F. balustinum (Vandamme During mass mortalities associated with granuloma et al., 1994). Flexibacter maritimus and F. ovolyticus tous lesions in various marine fish species from Florida should also be reclassified in a new genus, but their in 1951, an organism was isolated from sea water and generic epithet was maintained pending further taxo named "Flavobacterium piscicida" (Bein, 1954). Sub nomic investigations (Bernardet et al., 1996). Conse sequent investigations led to the reclassification of the quently, all fish pathogenic bacterial species within bacterium as "Pseudomonas piscicida" (Buck et al., rRNA superfamily V are now included in the family 1963), but it was then listed among the incertae sedis of Flavobacteriaceae, but only some of them exhibit a the genus Alteromonas to which it phenotypically gliding motility. resembles (Baumann et al., 1984). A phylogenetic study finally resulted in the allocation of this species to the new genus Pseudoalteromonas (Gauthier et al., Unidentified or doubtful pathogenic organisms 1995). Mortality could have resulted from a simulta "Sporocytophaga" sp. neous phytoplankton bloom ("red tide") rather than the Bacteria exhibiting microcyst-like structures have bacterium (B. Austin, personal communication), but a occasionally been observed in diseased marine fish, but certain toxicity of liquid cultures and their filtrates was identification of the pathogen is doubtful as no strain indeed demonstrated for several fish and crab species was ever isolated and very scant information is avail (Hansen et al., 1965). able (Pacha and Ordal, 1970; Wood, 1974; Austin and The most recent description of a "Flavobacterium" Austin, 1987). The most recent case report concerned like organism pathogenic for marine fish deals with Atlantic salmon smolt suffering from severe jaw ero a bacterium isolated during the summer of 1978 sion within 6 to 8 weeks of introduction into the ocean from coho salmon reared in sea water in Galicia, Spain (Hicks, 1989). Affiliation of the bacteria observed in (ACUIGROUP, 1980). The outbreak caused 20-25% fish lesions to the genus Sporocytophaga is most un mortality with signs of haemorrhagic septicaemia, and likely as the type and only valid species within this the bacterium was isolated from kidney and liver. Cytophaga/Flexibacter in marine fish 231 Clinical signs and 100% mortality resulted from intra rium involved in the Washington outbreak was not iso venous injection of a bacterial suspension, but the au lated (Frelier et al., 1994), and the organism causing the thors surmised that the virulence of the bacterium was disease in British Columbia was erroneously identified probably revealed by several factors such as high water as "Sporocytophaga" based on microscopic observation temperature, high density of fish population, and severe only (Hicks, 1989) (see above). A yellow organism fouling of cages with algae and mussel larvae. Generic growing on media containing seawater or at least 1% identification of the isolate was based on a rather scant NaCl was recovered
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