Vibrio Harveyi: a Serious Pathogen of Fsh and Invertebrates in Mariculture
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Marine Life Science & Technology (2020) 2:231–245 https://doi.org/10.1007/s42995-020-00037-z REVIEW Vibrio harveyi: a serious pathogen of fsh and invertebrates in mariculture Xiao‑Hua Zhang1,2,3 · Xinxin He1 · Brian Austin4 Received: 6 January 2020 / Accepted: 26 February 2020 / Published online: 3 April 2020 © The Author(s) 2020 Abstract Vibrio harveyi, which belongs to family Vibrionaceae of class Gammaproteobacteria, includes the species V. carchariae and V. trachuri as its junior synonyms. The organism is a well-recognized and serious bacterial pathogen of marine fsh and invertebrates, including penaeid shrimp, in aquaculture. Diseased fsh may exhibit a range of lesions, including eye lesions/blindness, gastro-enteritis, muscle necrosis, skin ulcers, and tail rot disease. In shrimp, V. harveyi is regarded as the etiological agent of luminous vibriosis in which afected animals glow in the dark. There is a second condition of shrimp known as Bolitas negricans where the digestive tract is flled with spheres of sloughed-of tissue. It is recognized that the pathogenicity mechanisms of V. harveyi may be diferent in fsh and penaeid shrimp. In shrimp, the pathogenicity mecha- nisms involved the endotoxin lipopolysaccharide, and extracellular proteases, and interaction with bacteriophages. In fsh, the pathogenicity mechanisms involved extracellular hemolysin (encoded by duplicate hemolysin genes), which was identifed as a phospholipase B and could inactivate fsh cells by apoptosis, via the caspase activation pathway. V. harveyi may enter the so-called viable but nonculturable (VBNC) state, and resuscitation of the VBNC cells may be an important reason for vibriosis outbreaks in aquaculture. Disease control measures center on dietary supplements (including probiotics), nonspecifc immunostimulants, and vaccines and to a lesser extent antibiotics and other antimicrobial compounds. Keywords Vibrio harveyi · Pathogen · Fish · Invertebrates · Aquaculture Introduction waters of Asia, southern Europe, and South America. How- ever, V. harveyi is not always recovered as a pure culture Vibrio harveyi, which occurs naturally in marine habitats from diseased animals. Instead, there is some evidence that (Firmino et al. 2019; Zhang et al. 2018), has developed into the pathogen may be recovered in mixed microbial popula- a signifcant pathogen of wild and cultured marine fsh and tions, with, for example, V. chagassi (Fabbro et al. 2011). invertebrates (notably penaeid shrimp), especially in warm Moreover, V. alginolyticus, V. harveyi, and V. parahaemo- lyticus were detected in diseased yellow croaker (Pseudosci- Edited by Xin Yu. aena crocea) in China; none of the three bacterial pathogens dominated (Liu et al. 2016). Similarly, V. harveyi was recov- * Xiao-Hua Zhang ered with V. alginolyticus from diseased hybrid groupers [email protected] (Epinephelus polyphekadion × E. fuscoguttatus) in Malaysia ( 1 MOE Key Laboratory of Marine Genetics and Breeding, Mohamad et al. 2019). Of course, it is uncertain whether College of Marine Life Sciences, Ocean University of China, the presence of two or more bacterial taxa from the same Qingdao 266003, China pathological material represents co-culture or the presence 2 Laboratory for Marine Ecology and Environmental of secondary invaders or even chance contaminants. Unfor- Science, Qingdao National Laboratory for Marine Science tunately, this aspect of pathology is rarely investigated. This and Technology, Qingdao 266237, China review strives to discuss the biology of V. harveyi particu- 3 Frontiers Science Center for Deep Ocean Multispheres larly aspects which appertain to its role as a serious pathogen and Earth System, Ocean University of China, of mariculture. Qingdao 266100, China 4 Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK Vol.:(0123456789)1 3 232 Marine Life Science & Technology (2020) 2:231–245 Taxonomy Vibrio harveyi was linked to V. campbellii by phenotyp- ing and genotyping (Gomez-Gil et al. 2004). They noted that Vibrio harveyi is a member of the genus Vibrio, in the family some isolates, which were labeled as V. harveyi, belonged Vibrionaceae, order Vibrionales, class Gammaproteobac- in V. campbellii. However, multilocus sequence analysis teria, and phylum Proteobacteria. The classifcation of the confrmed the distinctness of bona fde isolates of V. har- organism has progressed from its initial name of Achromo- veyi and V. campbellii, and verifed that both species are, bacter harveyi (E. N. Harvey was a pioneer in the systemat- indeed, separate entities (Thompson et al. 2007). Certainly, ics of bioluminescence; Johnson and Shunk 1936) to Luci- questions have been raised concerning the accuracy of iden- bacterium harveyi and Beneckea harveyi to the currently tifying vibrios within the Harveyi clade. This problem may accepted name, V. harveyi (Farmer et al. 2005). Identifca- refect on the associated studies discussed below (Hofmann tion of isolates has progressed from phenotypic, serologic et al. 2012; Ke et al. 2017; Urbanczyk et al. 2013). to genotypic or polyphasic, including the use of DNA:DNA Vibrio carchariae was named after recovery of an iso- hybridization when Ishimaru and Muroga (1997) confrmed late from a dead sandbar shark (Carcharhinus plumbeus) that pathogenic isolates from milkfsh (Chanos chanos) in (Grimes et al. 1984) and lemon sharks (Negraprion brevi- Japan were defnitely V. harveyi. A brief phenotypic descrip- rostris) (Colwell and Grimes 1984). However, detailed tion mentions that V. harveyi comprises Gram-negative, taxonomic examination, including the use of 16S rRNA fermentative rod-shaped bacteria, which require for sodium gene sequencing (Gauger and Gomez-Chiarri 2002), led to chloride for growth and are motile by polar fagella (Fig. 1a, the recognition that V. carchariae and V. harveyi are virtu- b). Growth occurs on TCBS (cholera agar = thiosulfate cit- ally identical, with the name of harveyi having precedence rate bile salts sucrose agar) (Fig. 1c; Farmer et al. 2005). (Farmer and Hickman-Brenner 1992; Gauger and Gomez- Some cultures are luminous (Fig. 1d). However, the pheno- Chiarri 2002; Pedersen et al. 1998). It is noteworthy that type may be changed by infection with the Vibrio harveyi isolates identifed as V. carchariae have been isolated from myovirus like bacteriophage (VHML) (Vidgen et al. 2006). humans, who was bitten by sharks (Pavia et al. 1989). By 16S rRNA gene or whole-genome sequencing, V. harveyi The fsh pathogen V. trachuri was named by Iwamoto is clearly a core species of Vibrio (Dorsch et al. 1992; Lin et al. (1995), but was deduced to be synonymous with V. et al. 2018). harveyi, with the latter having precedence in taxonomy (Thompson et al. 2002). These workers carried out a detailed polyphasic taxonomy study employing phenotyping, 16S rRNA gene sequencing, fluorescent amplified fragment length polymorphisms (FAFLP), and DNA:DNA hybridi- zation. The outcome was the realization that V. trachuri was highly related to V. harveyi. Generally, V. carchariae and V. trachuri have been recov- ered from diseased fsh, whereas V. harveyi was predomi- nantly recovered from invertebrates. Therefore, the com- bined taxon is especially signifcant as a pathogen of marine vertebrates and invertebrates. The diseases Vibrio harveyi has been linked with disease in a broad spec- trum of warm water fsh and invertebrates (Table 1). The list of hosts is extensive, and includes silvery black porgy (Acan- thopagrus cuvieri) and brown spotted grouper (Epinephelus tauvina) in Kuwait (Saeed 1995), common dentex (Dentex dentex) and farmed sole (Solea senegalensis) in Spain (Com- pany et al. 1999; Zorrilla et al. 2003), and farmed sea perch (Lateolabrax japonicus) and cage-reared grouper (Epinephe- Fig. 1 Morphology of Vibrio harveyi strains. a Growth of V. harveyi lus awoara) in China (Qin et al. 2006; Wang et al. 2002). VIB 391 on marine agar 2216E; luminescence of V. harveyi VIB b V. harveyi has been often associated with eye disease, for 391; c growth of V. harveyi VIB 645 on TCBS agar; d transmission electron microscopy of VIB 645 cells obtained from marine broth example in common snook (Centropomus undecimalis) culture. Scale = 1 μm (Kraxberger-Beatty et al. 1990), milkfsh (Chanos chanos) 1 3 Marine Life Science & Technology (2020) 2:231–245 233 Table 1 Diseases of marine vertebrates and invertebrates attributed to Vibrio harveyi Disease Host Geographical range Key references Fish Eye disease Common snook (Centropomus undeci- USA Kraxberger-Beatty et al. (1990) malis) Milkfsh (Chanos chanos) Philippines Ishimaru and Muroga (1997) Short sunfsh (Mola mola) Spain Hispano et al. (1997) Gastro-enteritis Grouper (Epinephelus coioides) Taiwan, China Yii et al. (1997) Various fsh, including black sea bream, Taiwan, China Lee et al. (2002); Liu et al. (2003) Japanese sea bass, yellowfn sea bream, and red drum Necrotizing enteritis Summer founder (Paralichthys den- USA Gauger et al. (2006); Sofentino et al. tatus) (1999) Nodules on operculum Tiger pufer (Takifugu rubripes) Japan Mohi et al. (2010) Scale drop and muscle necrosis Barramundi (Lates calcarifer) Vietnam Dong et al. (2017a) Hybrid grouper (Epinephelus fuscogut- China Zhu et al. (2018) tatus x E. lanceolatus) Skin ulcers Shark (Carcharhinus plumbeus) Italy Bertone et al. (1996) Sole (Solea senegalensis) Spain Zorrilla et al. (2003) Hybrid grouper (E. fuscoguttatus x E. China Shen et al. (2017) lanceolatus) Tail rot disease Sea perch (Lateolabrax japonicus) China Wang et al. (2002)