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Bacterial Diseases of Abalone

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Category

Category 4 (Negligible Regulatory Significance in Canada)

Common, generally accepted names of the organism or disease agent

Various bacterial diseases including juvenile vibriosis but not blister disease.

Scientific name or taxonomic affiliation

Vibrio spp. including Vibrio harveyi, Vibrio carchariae (a junior synonym of V. harveyi, Gauger and Gómez-Chiarri (2002)), Vibrio splendidus I, Vibrio alginolyticus, Vibrio parahaemolyticus, Vibrio campbellii, Vibrio tubiashii as well as other bacteria such as Clostridium lituseberense, Klebsiella oxytoca, Shewanella colwelliana, Francisella halioticida, Flavobacterium-like bacteria, long Flexibacter/Cytophaga-like rod bacteria and Pasteurella spp. During mass mortalities of farmed H. diversicolor supertexta in Taiwan, two strains of V. parahaemolyticus were isolated from the haemolymph of small abalone with signs of withering syndrome (Liu et al. 2000, Huang et al. 2001).Note that presence of the etiological agent of classical withering syndrome was not assessed in these studies). Also, Huang et al. (2001) claimed that V. parahaemolyticus is one of the causative agents of withering syndrome.

Vibrio fluvialis II has been described as the cause of blister (pustule) disease in abalone in China.

Geographic distribution

Abalone in culture facilities around the world including hatcheries in California, USA; Baja California, Mexico; Australia; New Zealand; Malaysia; China; Japan; and British Columbia, Canada. Bacterial disease was also associated with mass mortalities of wild abalone on the northern coast of France.

Host species

Haliotis rufescens, Haliotis kamtschatkana (Bower, S.M., unpublished records), Haliotis rubra, Haliotis laevigata, Haliotis tuberculata, Haliotis midae, Haliotis iris, Haliotis diversicolor, Haliotis diversicolor supertexta, Haliotis gigentea, Haliotis asinina and larval and juvenile bivalves under intensive culture including oysters, clams and scallops.

Impact on the host

Systemic infection of the soft-tissues of cultured juvenile abalone, resulting in tissue necrosis (due to production of exotoxin by the bacteria) and death. Vibrio spp. are usually not considered a problem for abalone larval culture because the larval period is relatively short and stringent sanitary practices are effective in avoiding potential problems. However, Anguiano-Beltrán et al. (1998) determined experimentally that Vibrio alginolyticus can cause massive mortality in larvae of Haliotis rufescens within 24 hours at concentrations above 105 bacteria per ml, while a concentration of 106 bacteria per ml was required to produce the same effect in 4 day old post-larval abalone. Lee et al. (2001) and Huang et al. (2001) reported that in laboratory experiments, small Haliotis diversicolor supertexta (about 10 to 14 g in weight) were more susceptible to strains of V. alginolyticus and/or Vibrio parahaemolyticus (originally isolated from the haemolymph of moribund small abalone of the same species) at warmer water temperatures (above 28 °C).

In China, various species of bacteria have been associated with disease in farmed abalone. Ma et al. (1996) identified Vibrio campbellii as the cause of septicopyaemia in Haliotis discus hannai. Zhang et al. (2001) reported that V. alginolyticus and V. parahaemolyticus were associated with a serious epidemic in farmed H. diversicolor supertexta in Dongshan Prefecture, Fujian Province. Also, V . parahaemolyticus was associated with mass mortalities of Haliotis diversicolor supertexta post-larvae on the south coast (Cai et al. 2006, 2007). Klebsiella oxytoca was associated with mass mortalities of post-larvae of the same species of abalone in Fujian, China (Cai et al. 2008). A Vibrio harveyi-related species was linked with the mass mortality of farmed adult H. diversicolor in Fujian, China (Jiang et al. 2013). Cheng et al. (2004a to e) addressed the immune response and susceptibility of farmed H. diversicolor supertexta to V. parahaemolyticus under various experimental conditions. They concluded that H. diversicolor supertexta transferred from 30% to 20, 25 and 35% salinity for 72 hours (Cheng et al. 2004a) or transferred from 28 °C to 32 °C for 72 hours (Cheng et al. 2004c) had reduced immune ability and decreased resistance against V. parahaemolyticus infection. In addition, H. diversicolor supertexta exposed to ammonia (3.16 mg per liter of ammonia-N) for 24 hours (Cheng et al. 2004b), to nitrite-N in water at concentrations as low as 0.96 mg per liter for 24 hours (Cheng et al. 2004d) or to hypoxia stress of dissolved oxygen as low as 3.57 and 2.05 mg per liter for 24 hours (Cheng et al. 2004e) caused a depression in immune parameters and an increase in mortality from V. parahaemolyticus infection. Shuhong et al. (2004) reported that farmed H. diversicolor supertexta injected with V. parahaemolyticus had increased innate immune factors (acid phosphate and alkaline phosphate) and a decrease in superoxide dismutase activity in their haemolymph by 24 hours after injection but there was no change in these three parameters in control abalone nor in abalone injected with Escherichia coli.

In Taiwan, Vibrio parahaemolyticus was isolated from small farmed H. diversicolor supertexta experiencing mass mortalities and displaying signs similar to the abalone disease called withering syndrome (Liu et al. 2000, Huang et al. 2001). One of the isolates and its extracellular products were virulent to small abalone with LD50 values of 1.6 X 105 colony-forming units and 7.58 µg protein per gram body weight, respectively (Liu et al. 2000).

In Tasmania, Australia, disease outbreaks among cultured abalone (Haliotis rubra, H. laevigata and their hybrids) were associated with two species of Vibrio (V. harveyi and V. splendidus I) and Flavobacterium-like bacterium. In most cases, stress factors (e.g., high temperatures, grading trauma, anesthetics, gradual increase in salinity in the recirculation system, etc.) were reported to have precipitated the diseases (Handlinger et al. 2001, 2002, 2005). Dang et al. (2011a) found considerable variability in the in vitro levels of antibacterial activity towards Vibrio harveyi in haemolymph of Haliotis rubra, Haliotis laevigata and their hybrid cross.

In New Zealand, up to 45% of the Haliotis iris cultured at high densities had lesions of erosion and exfoliation of the epithelium of the foot and epipodium that were usually associated with infections of various bacteria (Diggles and Oliver 2005).

In Japan, Vibrio harveyi (=carchariae) was isolated from cultured Haliotis (=Sulculus) diversicolor supratexta experiencing a mass mortality in Kanagawa Prefecture. In this case, white spots consisting of necrotic muscle fibers and bacteria on the abalone foot accompanied by high mortalities were characteristic of the disease (Nishimori et al. 1998). In Shimane Prefecture, a mass mortality (84%) of Haliotis (=Nordotis) gigantea on a private abalone farm was associated with the facultative intracellular bacterium Francisella halioticida (Kamaishi et al. 2010, Brevik et al. 2011). In this case, there were no notable clinical signs but infected abalone lost adhesive strength, often lay upside down on the bottom of the tanks and eventually died (Kamaishi et al. 2010).

In France, Vibrio harveyi (=carchariae) was also identified as the probable cause of mass mortalities of adult Haliotis tuberculata in the natural environment along the Brittany and Normandy coasts of France and in a land-based abalone farm in Normandy (Nicolas et al. 2002, Huchette and Clavier 2004). Travers et al. (2008a) found a rare pathogenic strain of V. harveyi responsible for epizootic mass mortalities of H. tuberculata in France at the end of the summers, between 1998 and 2005, with the highest mortalities among mature abalone at temperatures above 19 °C. The highly virulent ORM4 strain of V. harveyi harboured a 9.6 kb plasmid named pVCR1 suggesting its involvement in the virulent phenotype (Schikorski et al. 2013). Travers et al. (2008b) reported a clear concordance between the maturation and spawning processes and immune status of H. tuberculata regarding susceptibility to V. harveyi. The large losses of reproductively mature abalone coincided with thermal maxima, and the relationship between temperature and vibriosis was demonstrated in both laboratory trials and field studies (Travers et al. 2009a). In laboratory experiments, a 1 °C increase in temperature (from 17 °C to 18 °C) resulted in an increase in losses from 0% to 80% when abalones were exposed to the bacterium during their spawning season (Travers et al. 2009a). Thus, susceptibility to this pathogen is driven by both climatic factors and reproductive physiology (Burge et al. 2014).

Travers et al. (2009b) suggested that modulation of p38 MAPKs, a mitogen-activated protein kinases, by virulent strains of V. harveyi may be one of the ways used to attack H. tuberculata and escape the abalone haemocyte immune response. The molecular technique of constructing suppression subtractive hybridization (SSH) cDNA libraries was used to identify potential candidates for investigations into the functional basis of resistance and susceptibility to summer vibriosis outbreaks in H. tuberculata (Travers et al. 2010). In the laboratory, Cardinaud et al. (2015) determined that V. harveyi invaded the circulatory system of H. tuberculata a few hours after exposure and was lethal after 2 days of infection. In this study, they observed, over the first 24 hours of infection, an initial induction of immune gene expression (including Rel/NF-kB, Mpeg and Clathrin), rapidly followed by a significant immunosuppression characterized by reduced cellular haemocyte parameters, immune response gene expressions and enzymatic activities. These immune function alterations including haemolytic activity were positively correlated with V. harveyi concentration (Cardinaud et al. 2015).

Also in France, Vibrio splendidus was associated with the mortality of Haliotis tuberculata (Saulnier et al. 2010) and a strain of Vibrio tubiashii was isolated from H. tuberculata during a mortality episode of H. tuberculata in Normandy (Travers et al. 2014).

Diagnostic techniques

Gross Observations

In diseased Haliotis asinina (with systemic bacterial infections of Gram-negative bacterial rods with a presumptive identification to the genera Vibrio spp. and Pasteurella spp.), ulcer-like lesions of the tegument with white patches at the foot margins often occurred. In the most severe cases, the mantle was attached loosely to the shell with development of a white pseudomembrane in some instances (Kua et al. 2011). Diseased post-larvae of Haliotis diversicolor supertexta infected with Vibrio parahaemolyticus turned white in colour and fell off of the diatom films on which they were being cultured (Cai et al. 2007). In small H. diversicolor supertexta (about 5 cm in shell length) infected with V. parahaemolyticus, the gross signs of disease were reminiscent of withering syndrome including shrunken foot muscle, discoloration of the epipodium and retraction of visceral tissues (Huang et al. 2001).

Histology

Indication of tissue necrosis and the presence of rod-shaped bacteria (usually slightly curved) within the tissues were observed. Kua et al. (2011) illustrated a systemic bacterial infection with intense haemocytic infiltrations and abscess-like lesions in the foot muscle of Haliotis asinina.

Culture

Colonies of Vibrio spp. were isolated and cultured (TCBS bacterial culture agar) from the tissues of sick abalone. A pathogenic strain of V. harveyi (ORM4) was green fluorescent protein-tagged and validated both for its growth characteristics and for its virulence as a genuine model for abalone disease (Travers et al. 2008c). Travers et al. (2008c) indicated that the fluorescent-tagged strain allows V. harveyi quantification by flow cytometry in seawater and in abalone haemolymph as well as the in situ detection of the parasite inside abalone tissues. Pichon et al. (2013) used this tagged strain to help visualise the interactions between V. harveyi and primary cell cultures from abalone gill tissue.

Electron Microscopy

Pichon et al. (2013) used transmission electron microscopy to detect internalized bacteria within the cytoplasm of haemocytes and epithelial cells in primary cell cultures from abalone gill tissue exposed to V. harveyi in vitro. In infected cells, they found condensed mitochondria in a hyperphosphorylation oxydative state and lysosomes indicating high activity induced by bacterial phagocytosis and endocytosis in vitro (Pichon et al. 2013).

DNA Probes

Accurate identification of vibrios at the family and genus levels is obtained by 16S rRNA gene sequencing, whereas identification at the species and strain levels requires the application of genomic analyses, including DNA-DNA hybridization, repetitive extragenic palindromic polymerase chain reaction, amplified fragment length polymorphism analysis, and analysis of sequence fragments from various gene loci (Thompson et al. 2004, 2005). For example, Vibrio harveyi can be differentiated from closely related species of Vibrio by toxR gene sequence analysis using toxR-targeted polymerase chain reaction (PCR) primers that amplify a 390 base-pair fragment of the gene (Conejero and Hedreyda 2003). Because these techniques are time consuming and not well adapted for the performance of rapid diagnostic tests in the context of disease surveillance and prevention in aquaculture facilities, Schikorski et al. (2013) developed two TaqMan real-time PCR (quantitative PCR (qPCR)) assays, one to specifically target V. harveyi and the other to exclusively target the pVCR1 plasmid (associated with pathogenicity of V. harveyi). By combining both assays in a duplex procedure, the rapid and specific detection (in less than two hours) and quantification of both V. harveyi and the presence of plasmid pVCR1 was accomplished with unidentified bacterial colonies isolated in vitro and in the haemolymph of abalone or its surrounding seawater. This qPCR assay targeting V. harveyi was used to monitor V. harveyi ORM4 strain in experimentally infected H. tuberculata (Schikorski et al. 2013).

Methods of control

Vibrio bacteria are ubiquitous, hence eradication of the aetiological agent is impossible. Vibriosis appears to be directly related to poor husbandry and other stressful conditions that predispose the abalone to infection. Sources of infection are broodstock, food supply (e.g., algal cultures), surfaces utilized by abalone, incoming sea water and air-borne contaminants (Lizárraga-Partida et al. 1998). In order to alleviate the problem, the source of infection should be determined by culturing bacteria from the above possible sources. For example, Kua et al. (2011) determined that mortalities associated with severe enteritis among farmed Haliotis asinina in Malaysia was attributed to systemic bacterial infection by Gram-negative bacterial rods with a presumptive identification to the genera Vibrio spp. and Pasteurella spp. They found that the disease was transmitted from the seaweed (Gracilaria changii) used as food for the abalone. The Gracilaria changii stock was procured from abandoned shrimp ponds located on the north western coasts of the Malaysian Peninsula. This case study highlights the importance of good farming and management practices and as well as appropriate abalone husbandry procedures (Kua et al. 2011).

Vibriosis can also be avoided by limiting the exposure of cultured abalone to physical and chemical stresses (Elston and Lockwood 1983). Stress factors that precipitate disease should be identified and disease control can be directed towards eliminating the stress (Handlinger et al. 2005). Dang et al. (2011b) suggested that diet may enhance antibacterial activity against Vibrio anguillarum in at least farmed Haliotis laevigata. Culturing larvae under optimal conditions (i.e., suitable temperature and salinity for the abalone species) and the use of sterilised seawater (e.g., irradiated with ultraviolet light) can reduce the development of vibriosis. Batches of abalone containing infected individuals should be destroyed in an approved manner followed by disinfection of all containers and equipment in contact with the infected stock.

Dixon et al. (1991) reported that exposure to ozonated water and treatment (bath and injection) with a broad spectrum antibiotic was effective against bacterial infections (caused by Clostridium lituseberense or Vibrio alginolyticus) in some abalone (Haliotis midae) in a South African experimental facility. However, Handlinger et al. (2002, 2005) found antibiotic use to give equivocal results on bacterial infections in Tasmanian farmed abalone. Also, Anguiano-Beltrán and Searcy-Bernal (2007) reported that antibiotic treatment slowed post-larval growth and reduced survival of H. rufescens and suggested that bacteria were important to nutrition and/or digestion of abalone post-larvae.

References

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Citation Information

Bower, S.M. (2017): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Bacterial Diseases of Abalone.

Date last revised: December 2017
Comments to Susan Bower

Date modified: