Tenacibaculosis infection in marine fish caused by Tenacibaculum maritimum: a review

Abstract

Tenacibaculum maritimum is the aetiological agent of an ulcerative disease known as tenacibaculosis, which affects a large number of marine fish species in the world and is of considerable economic significance to aquaculture producers. Problems associated with epizootics include high mortality rates, increased susceptibility to other pathogens, high labour costs of treatment and enormous expenditures on chemotherapy. In the present article we review current knowledge on this bacterial pathogen, focusing on important aspects such as the phenotypic, serologic and genetic characterization of the bacterium, its geographical distribution and the host species affected. The epizootiology of the disease, the routes of transmission and the putative reservoirs of T. maritimum are also discussed. We include a summary of molecular diagnostic procedures, the current status of prevention and control strategies, the main virulence mechanisms of the pathogen, and we attempt to highlight fruitful areas for continued research. TAXONOMYThe taxonomy of Tenacibaculum maritimum was a matter of controversy and confusion for decades, and it has only recently been clarified by Suzuki et al. (2001). Masumura & Wakabayashi (1977) isolated a gliding bacterium that had caused mass mortalities among certain cultured marine fish. These strains were characterized by Hikida et al. (1979), who announced their intention to make a separate formal proposal of the name Flexibacter marinus. Since the epithet marinus had already been used in the name Vibrio marinus, the authors changed their mind on the use of this epithet, and the eventual formal proposal was a taxon called Flexibacter maritimus (Wakabayashi et al. 1986, Holmes 1992. Reichenbach (1989) listed the pathogen as Cytophaga marina, but the priority of the name Flexibacter maritimus was later recognized (Holmes 1992). These results were confirmed by Bernardet & Grimont (1989), who also validated the name Flexibacter maritimus based on DNA-DNA hybridisation methods.However, the resolution of phenotypic characterization and 16S ribosomal RNA (rRNA) sequence analysis is insufficient to distinguish closely related organisms. Thus, Suzuki et al. (2001), based on the nucleotide sequence of the gyrB, proposed that Flexibacter maritimus should be transferred to the new genus Tenacibaculum, in which 7 members are currently included. Table 1 shows the main differential characteristics of the described species of the genus Tenacibaculum. GEOGRAPHICAL DISTRIBUTION AND HOST SPECIESThe geographical distribution of Tenacibaculum maritimum in wild and farmed fish is shown in Table 2. 256 Characteristic T. maritimum T. ovolyticum T. mesophilum T. amilotyticum T. skagerrakense T. lutimarisOrigin Diseased red sea Halibut egg, Sponge and Macroalgae, Pelagic, Tidal flat, bream fingerling, Japan Norway macroalgae, Japan Japan Denmark Korea Cells size (µm) 2-30 × 0.5 2-20 × 0.5 1.5-10 × 0.5 2-4 × 0.4 2-15 × 0.5 2-10 × 0. Percentage of NaCl in the medium Table 1. Differential phenotypic characteris...

Identification of Vibrio harveyi isolated from diseased cultured wedge sole Dicologoglossa cuneata

“…The lack of susceptibility of wedge sole to bath immersion may be associated with the absence of other determining factors, such as previous stressful situations, skin lesions or infections. In this sense, it is important to note that most strains were isolated together with Tenacibaculum maritimum or T. soleae strains, proven pathogens for flatfishes (Avendaño-Herrera et al 2006b, Piñeiro-Vidal et al 2008. …”

Multilocus Sequence Analysis of the Marine Bacterial Genus Tenacibaculum Suggests Parallel Evolution of Fish Pathogenicity and Endemic Colonization of Aquaculture Systems

“…The best known of the pathogens in this genus, T. maritimum (3), has been repeatedly identified as a cause of high levels of mortality and economic losses in many cultured marine fish species worldwide (4). The disease, often referred to as tenacibaculosis, typically consists of external lesions and necrosis that can affect virtually all areas of the body surface (5).…”

Isolation of Lacinutrix venerupis strains associated with disease outbreaks in sea bream Sparus aurata and European sea bass Dicentrarchus labrax

“…Opportunistic diseases are triggered when hosts are stressed, and temperature also plays an important role because of its influence on the prevalence of the pathogen and on the immune response in fish; on the other hand, high population densities in aquaculture facilities not only cause stress, but also contribute to the spread of the infection (Hurst 2016). An example of an opportunistic pathogen within the family Flavobacteriaceae is T. maritimum, which displays an increased prevalence and severity at temperatures above 15°C, with low water quality, stressful conditions (high density, poor feeding, excess of UV light) or with bad skin conditions (Avendaño-Herrera et al 2006). On the other hand, since intraperitoneal injection is not a natural route of infection, more work is needed to investigate the susceptibility of sea bass and sea bream to L. venerupis under more natural conditions.…”

“…Some members of this family are well known fish pathogens, including Flavobacterium psychrophilum, which is responsible for 'cold water disease' in salmonids (Starliper 2011), F. columnare, which causes 'columnaris disease' in freshwater fish (Declercq et al 2013), and Tenacibaculum maritimum, described in a variety of marine fish as being responsible for 'black patch necrosis' or 'flexibacteriosis' (Toranzo et al 2005, Avendaño-Herrera et al 2006. Many more species of this family have been associated with disease in fish, some of which have been described only recently, such as Chryseobacterium piscicola and T. dicentrarchi in salmonids (Ilardi et al 2009, Starliper 2011, Piñeiro-Vidal et al 2012, Avendaño-Herrera et al 2016 or T. soleae, associated with disease in a number of flatfish species (Piñeiro-Vidal et al 2008, López et al 2010.…”