Contrasting outcomes of Vibrio harveyi pathogenicity in gilthead seabream, Sparus aurata and European seabass, Dicentrachus labrax
Introduction
Vibrio spp. are ubiquitous in the marine environment, particularly in tropical and temperate waters, representing the major bacterial pathogens affecting development of fish farming (Austin and Austin, 2012; Vandenberghe et al., 2003; Zorrilla et al., 2003a), especially in the Mediterranean Sea (Pujalte et al., 2003a). One of the most commonly isolated marine Vibrio species, Vibrio harveyi [syn. V. carchariae] (Gauger and Gómez-Chiarri, 2002) is a marine Gram-negative bioluminescent bacteria with a requirement for sodium chloride (Farmer et al., 2005). The species has been described as free-living, associated to some microalgae blooms, or associated to the intestinal microbiota (Makemson and Hermosa, 1999; Miller et al., 2005; Ramesh et al., 1990). V. harveyi has also been reported during warm seasons, as the dominant heterotrophic bacterial species in western Mediterranean coastal areas (Arias et al., 1999; Ortigosa et al., 1994; Pujalte et al., 1999) and elsewhere, that can be present in expansive blooms (e.g. 15,400 km2 of sea surface) in association with species of microalgae (Miller et al., 2005). Moreover, it is recognized as an economically significant pathogen for the aquaculture industry (Cano-Gomez et al., 2009), with some sporadic cases of wound infections in humans also reported (Austin, 2010; Del Gigia-Aguirre et al., 2017).
As a serious pathogen affecting the aquaculture industry V. harveyi has effected many marine vertebrate and invertebrates (Austin and Zhang, 2006), and is frequently isolated from marine bivalves with implications in some mass mortalities of shellfish (Pass et al., 1987; Sawabe et al., 2007; Travers et al., 2008). Additionally, some studies have described V. harveyi as pathogenic for several species of crustacean larvae (Diggles et al., 2000; Karunasagar et al., 1994; Lavilla-Pitogo et al., 1990; Liu et al., 1996; Robertson et al., 1998; Vandenberghe et al., 1999). Moreover, it has also been associated to several opportunistic infections in fish, and responsible for several cases of infectious necrotizing enteritis, which is characterized by redness of the anal area, abdominal swelling with accumulation of ascitic fluid, inflammation of the anterior intestine and necrosis of the posterior intestine (Austin and Zhang, 2006). Several cultured fish species with economic relevance are globally affected, such as rainbow trout (Oncorhynchus mykiss), Atlantic salmon (Salmo salar L.) (Zhang and Austin, 2000), Senegalese sole (Solea senegalensis) (Zorrilla et al., 2003a), Japanese seabass (Lateolabrax japonicus) (Lee et al., 2002), cobia (Rachycentron canadum) (Liu et al., 2004b), common dentex (Dentex dentex) (Company et al., 1999; Pujalte et al., 2003b), among others.
Gilthead seabream, Sparus aurata and European seabass, Dicentrarchus labrax are presently the dominant fish species cultured along the Mediterranean coast (FAO, 2005-2018). Infections and mortality episodes observed in cultured seabream and seabass seem to be the result of the interaction of several factors such as poor water quality, seasonality, age-related host susceptibility, stress and pathogen virulence (Abdel-Aziz et al., 2013; Austin and Austin, 2012). Moreover, both fish species are often cultivated at the same farms or in very close proximity. Therefore, it is very relevant to assess the level of risk posed by pathogens, which are sharing tank facilities or where both fish species coexist in the same water masses.
Several bacterial species have been described as common pathogens in cultured gilthead seabream (Balebona et al., 1998; Rodgers and Furones, 1998; Toranzo et al., 2005). The genus Vibrio includes opportunistic pathogens that can affect cultured gilthead seabream (Balebona et al., 1998; Haldar et al., 2010) and European seabass (Pujalte et al., 2003b). Pujalte et al. (2003a) reported V. harveyi as the most frequent species recovered from diseased and asymptomatic gilthead seabream cultured in the Spanish Mediterranean area, from larval to commercial sizes. Disease outbreaks due to V. harveyi exhibit clear seasonal variation with increased prevalence coinciding with temperatures above 20 °C (Arias et al., 1999; Pujalte et al., 1999) and it was also suggested that its increased prevalence could lead to co-infection of other bacterial pathogens (Pujalte et al., 2003a). Furthermore, in a recent study, Scarano et al. (2014) demonstrated that gilthead seabream reared in sea cages are a potential source of Vibrio spp. exhibiting resistance against the most commonly used antibiotics. Recently, in a survey assessing the main pathogens threatening aquaculture in the Mediterranean (Vendramin et al., 2016), V. harveyi was recognized as an emerging problem in seabass.
Although bacterial infections in fish farming systems are common, the present study was designed to determine and compare differences in susceptibilities of the two most important fish species in the Mediterranean aquaculture, Gilthead seabream (S. aurata) and European seabass (D. labrax), to a strain of Vibrio harveyi isolated from cultured seabream during a separate previous nutritional trial. This study aimed to assess the risk and the vulnerability of these two species to this strain of V. harveyi encountered in a naturally occurring epizootic event. Additionally, an attempt to attenuate virulence using serial passage on laboratory media was also performed to compare with the virulence observed using the native isolate.
Section snippets
Fish rearing conditions
During October and November of 2017, over the course of a nutritional assay at IRTA facilities (Sant Carles de la Ràpita), located in the western Mediterranean (Tarragona, Spain), some isolated cases of abdominal swelling with an accumulation of ascitic fluid were observed in cultured juveniles of gilthead seabream (mean ± SD; 15.0 ± 0.5 cm length; mean body weight 81.3 ± 3.8 g), with a cumulative mortality of 3%. Initially, fish were stocked in 200 L tanks at a density of 2 kg m−3 under
Pathogen characterization and identification
All bacterial isolates from ascitic fluid of diseased gilthead seabream were Gram negative rods (~1.5 μm × 0.8 μm). On TSA-NaCl plates, colonies were pale cream-colored with a raised center and peripheral swarm rings. On TCBS agar media, the colonies appeared yellow with crenellated edges. The 16S rDNA sequences were compared to the online database GenBank using the BLAST utility and multiple V. harveyi strains were identified as having identical sequences. From this result, the species was
Discussion
Many of the mortalities described in seabreams cultured in the Mediterranean and Atlantic areas have been associated with epizootic events related to vibriosis, including etiology by V. harveyi. In general, this disease in intensive culture systems is characterized by systemic haemorrhagic septicemia with marked abdominal swelling. Internally, congested blood vessels, branchial, hepatic and intestinal hemorrhages and ascites are the most common histopathological signs of this bacterial disease
Acknowledgements
This work has been supported by the project “Nutritional strategies for the improvement of productive performance: the use of functional feeds and health diets in aquaculture (DIETAplus)”, funded by JACUMAR (Ministry of Agriculture, Fisheries and Environment of Spain, MAPAMA) and FEMP (EU), and the MedAID project (Grant agreement No 727315), funded by the European Union‘s Horizon 2020 research and innovation program. Joana P. Firmino have been subsidized by the Industrial PhD program of the
References (56)
- et al.
Identifying some pathogenic Vibrio/Photobacterium species during mass mortalities of cultured gilthead seabream (Sparus aurata) and European seabass (Dicentrarchus labrax) from some Egyptian coastal provinces
Int. J. Veter. Sci. Med.
(2013) - et al.
Mutation and recombination in pathogen evolution: relevance, methods and controversies
Infect. Genet. Evol.
(2018) Vibrios as causal agents of zoonoses
Vet. Microbiol.
(2010)- et al.
Survey of bacterial pathologies affecting farmed gilt-head sea bream (Sparus aurata L.) in southwestern Spain from 1990 to 1996
Aquaculture
(1998) - et al.
Molecular identification, typing and tracking of Vibrio harveyi in aquaculture systems: current methods and future prospects
Aquaculture
(2009) The accumulation of deleterious genes in a population—Muller's ratchet
Theor. Popul. Biol.
(1978)- et al.
Identification of Vibrio harveyi as a causative bacterium for a tail rot disease of sea bream Sparus aurata from research hatchery in Malta
Microbiol. Res.
(2010) - et al.
Mass mortality of Penaeus monodon larvae due to antibiotic-resistant Vibrio harveyi infection
Aquaculture
(1994) - et al.
Occurrence of luminous bacterial disease of Penaeus monodon larvae in the Philippines
Aquaculture
(1990) - et al.
Numerical taxonomy of Vibrionaceae isolated from oysters and seawater along an annual cycle
Syst. Appl. Microbiol.
(1994)
Investigations into the causes of mortality of the pearl oyster, Pinctada maxima (Jamson), in Western Australia
Aquaculture
Virulence and molecular typing of Vibrio harveyi strains isolated from cultured dentex, gilthead sea bream and European sea bass
Syst. Appl. Microbiol.
A review of the main bacterial fish diseases in mariculture systems
Aquaculture
Summer immune depression associated with increased susceptibility of the European abalone, Haliotis tuberculata to Vibrio harveyi infection
Fish Shellfish Immunol.
Phenotypic diversity amongst Vibrio isolates from marine aquaculture systems
Aquaculture
The innate immune response of finfish - a review of current knowledge
Fish Shellfish Immunol.
Bacteria recovered from diseased cultured gilthead sea bream (Sparus aurata L.) in southwestern Spain
Aquaculture
Low incidence of Vibrio vulnificus among Vibrio isolates from sea water and shellfish of the western Mediterranean coast
J. Appl. Microbiol.
Vibrionaceae representatives
Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates
Lett. Appl. Microbiol.
Emerging Vibrio risk at high latitudes in response to ocean warming
Nat. Clim. Chang.
Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens
Proc. Natl. Acad. Sci.
Updated of the pathologies affecting cultured gilthead seabream, Sparus aurata
Annals Aquacult. Res.
Bacterial and parasitic pathogens in cultured common dentex, Dentex dentex L
J. Fish Dis.
Luminous vibriosis in rock lobster Jasus verreauxi (Decapoda: Palinuridae) phyllosoma larvae associated with infection by Vibrio harveyi
Dis. Aquat. Org.
Bacteriological and histopathological studies on Vibrio species isolated from naturally infected freshwater fish in Delta region, Egypt
Adv. Animal Veter. Sci.
National Aquaculture Sector Overview. Visión general del sector acuícola nacional - España
Bergey's manual® of systematic bacteriology
Cited by (37)
Transcriptome analysis of digestive diverticula of Hong Kong oyster (Crassostrea hongkongesis) infected with Vibrio harveyi
2023, Fish and Shellfish ImmunologyHepcidin and piscidin modulation and antibacterial response in gilthead seabream (Sparus aurata) infected with Vibrio harveyi
2023, Fish and Shellfish Immunology