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. 2020 Aug 7;9(8):493. doi: 10.3390/antibiotics9080493

Table 2.

A selection of phages reported for the biocontrol of pathogens in aquaculture.

Phage/Phages Cocktails
(Family)		 Target Microorganism Fish or Aquaculture Product Disease Relevant Achievements Reference
PLgY-16, PLgY-30, PLgW-1
(Siphoviridae)		 Lactococcus garvieae Yellowtail
(Seriola quinqueradiata)		 Lactococcosis

  • Isolation of new phages: PLgY-16 and PLgY were obtained from cultures of L. garviae isolated from diseased yellowtail; PLgW-1 was isolated from natural seawater

  • According to the results, anti-L. garvieae phage (administered orally or intraperitoneally) protected fish from experimental L. garvieae infection

 [49]
PPpW-3
(Podoviridae)
PPpW-4
(Myoviridae)
and a mixture of PPpW-3/W-4		 Pseudomonas plecoglossicida PTH-9802 strain Ayu fish
(Plecoglossus altivelis)		 Bacterial hemorrhagic ascites disease

  • Phages inhibited in vitro the growth of P. plecoglossicida. The highest inhibitory activity was shown by the mixture

  • In a field trial, when phage PPpW-3/W-4 was supplied with the food to ayu in a pond where the disease occurred naturally, fish mortality decreased to one-third after a 2 week period

 [105]
Viha8, Viha10 (Siphoviridae)
Viha9, Viha11		 Vibrio harveyi Shimp larvae
(Penaeus monodon)		 Luminescent vibriosis

  • Isolation of new phages: three from oyster tissue and one from shrimp hatchery water

  • Phage Viha10 was effective in reducing the population of V. harveyi in the biofilm formed on a high density polyethylene surface

  • In hatchery trials, the application of phage treatment (Viha8 and Viha10) resulted in 85% survival of P. monodon larvae

 [106]
Viha 1, Viha 2, Viha 3,Viha 5, Viha 6, Viha 7
(Siphoviridae)
Viha4
(Myoviridae)		 Vibrio harveyi Penaeid shrimp Luminescent vibriosis

  • Isolation of new phages from shrimp farms, hatcheries, and tidal creeks along the east and the west coasts of India

  • Phages were found to be highly lytic for V. harveyi. Six of them had a broad lytic spectrum, thus they could be potential candidates for biocontrol of this bacterium in aquaculture systems

 [107]
VhCCS-01, VhCCS-02, VhCCS-04, VhCCS-06, VhCCS-17, VhCCS-20
(Siphoviridae)
VhCCS-19, VhCCS-21
(Myoviridae) 		Vibrio harveyi Phyllosoma larvae of the tropical rock lobster
(Panulirus ornatus)		 Luminescent vibriosis

  • Isolation of new phages from water samples from discharge channels and grow-out ponds of a prawn farm in northeastern Australia

  • The host range for purified phage included V. harveyi, V. campbellii, V. rotiferianus and V. parahaemolyticus

  • The lytic ability of the isolated phages suggested that they are appropriate for phage therapy

 [108]
vB_VhaS-a, vB_VhaS
(Siphoviridae)		 Vibrio harveyi Abalone
(Haliotis laevigata).		 Vibriosis

  • Isolation of new phages from water or tissue sample liquid

  • In in vitro assays, the phages showed different antimicrobial abilities towards different V. harveyi isolates

  • In the bioassay, the treatment with phage resulted in 70% of abalone survival, as compared to the 0% exhibited by the positive bacterial control

 [109]
pVp-1
(Siphoviridae)		 Vibrio parahaemolyticus Oysters Luminescent vibriosis

  • Both by bath immersion and oyster surface-application, the lytic phage effectively reduced the bacterial growth of a multiple-antibiotic-resistant V. parahaemolyticus pandemic strain

 [110]
vB_VpS_BA3, vB-VpS_ CA8
(Siphoviridae)		 Vibrio parahaemolyticus - -

  • Isolation of new phages from sewage collected in Guangzhou, China

  • Taking into account the determined host range and the rate of inactivation in the in vitro phage-killing assay, phages, particularly CA8, had the potential to be used in phage therapy

 [111]
ΦVP-1
(Myoviridae)		 Multiple-drug-resistat Vibrio parahaemolyticus and Vibrio alginolyticus Penaeid shrimp Antibiofilm activity

  • Isolation of a new phage from shrimp pond water samples collected from aquafarms in Cochin, India

  • Ability to infect multiple-drug-resistant strains of mangrove and seafood origin belonging to the species V. parahaemolyticus and V. alginolyticus, and showing also biofilm reducing capacity

 [112]
309, ALMED, CHOED, ALME, CHOD, CHOB Vibrio anguillarum Fish
Atlantic salmon
(Salmo salar)		 Hemorrhagic septicemia

  • Isolation of new phages from bivalve samples purchased in the central market of Santiago, Chile

  • The phages exhibited ability to infect both V. anguillarum and V. ordalii but not V. parahaemolyticus strains

  • In both experimental tanks and fish farm assays, the CHOED phage was able to protect Salmo salar against experimentally induced vibriosis

 [113]
vB_VspP_pVa5
(N4-like podovirus)		 Vibrio splendidus Fish and bivalves Severe epizootics
Skin Ulceration Syndrome (SUS)

  • Isolation of a new phage from a sea-cage aquaculture farm in Greece with a very specific host range infecting only the bacterial host

  • The phage showed an intense bactericidal activity being proposed as a potential candidate for phage cocktails, suitable for the biological control of V. splendidus

 [114]
pVco-14
(Siphoviridae)		 Vibrio coralliilyticus Pacific oyster larvae
(Crassostrea gigas)		 Massive mortality of Pacific oyster larvae

  • Isolation of a new phage from the sewage at the oyster hatchery located at Tongyeong, Korea that specifically infects V. coralliilyticus

  • Oyster larvae pre-treated with phage pVco-14 before the bacterial challenge exhibited significantly higher survival rate when compared to the untreated groups

 [115]
ValLY-3, VspDsh-1, VspSw-1, VpaJT-1, and ValSw4-1
(Siphoviridae)		 Vibrio sp.
Va-F3 strain		 Shrimp
(Litopenaeus vannamei)		 Vibriosis

  • Isolation of new phages from wastewater samples collected from sewage draining exits in the cities of Shenzhen, Zhanjiang, and Shanwei, China

  • A workflow of preparing a phage cocktail was described: the phage cocktail preparation showed in vitro higher efficiency in inhibiting the growth of Vibrio sp. Va-F3 than any single phage

  • In in situ experiments, the survival rate of the group of shrimp treated with the cocktail was comparable to that of the group treated with antibiotics

 [116]
Different bacteriophages Aeromonas hydrophila and Edwardsiella tarda Japanese eel
(Anguilla Japonica)		 Hemorrhagic septicaemia and edwardsiellosis

  • Isolation of new phages from water samples in southern Taiwan

  • In pure culture, the phages decreased the bacterial host by three orders of magnitude after two hours

  • In pond water, phage treatment reduced 250-fold the A. hydrophila population in 8 h, while phage population increased

 [117]
Φ2, Φ5
(Myoviridae)		 Aeromonas hydrophila Catfish
(Pangasianodon hypophthalmus) 		Motile
Aeromonas Septicemia (MAS)

  • Isolation of new phages from water samples from the Saigon River of Ho Chi Minh City, Vietnam

  • Phages exhibited broad activity spectra, including multiple-antibiotic-resistant Aeromonas isolates

  • Phage treatments applied to infected catfish resulted in a significant increase in the survival rates when compared to control experiments

 [118]
Akh-2
(Siphoviridae)		 Aeromonas hydrophila Loach
(Misgurnus anguillicaudatu)		 Septicemia

  • Isolation of a new phage from water collected from Wahyeon Beach, Geoje Island, South Korea

  • In an experiment where the disease was artificially induced, loach treated with phage Akh-2 exhibited an increased survival rate as compared with the untreated control

 [119]
HER 110
(Myoviridae)		 Aeromonas salmonicida
HER 1107 strain		 Brook trout
(Oncorhynchus
fontinalis)
formerly, (Salvelinus fontinalis) 		Furunculosis

  • In aquarium assays, treatment with phage HER 110 declined the population of A. salmonicida in 3 days and additionally, the onset of furunculosis in brook trout was delayed by 7 days.

  • Different phages were active against A. salmonicida HER 1107. The mutants that developed resistance to phage HER 110 were sensitive to other phages

 [120]
PAS-1 Aeromonas salmonicida Rainbow trout
(Oncorhynchus mykiss)		 Furunculosis

  • The phage showed in vitro efficient bacteriolytic activity against A. salmonicida subsp. salmonicida strain AS05

  • In tank experiments, the administration of phage PAS-1 to A. salmonicida subsp. salmonicida-infected rainbow trout exhibited notable protective effects, increasing survival rates and mean times to death

 [121]
AS-A
AS-D
AS-E
Cocktails combining two or three phages		 Aeromonas salmonicida - Furunculosis

  • Isolation of new phages from sewage network of Aveiro, Portugal

  • Phage cocktails developed

  • Phage cocktails reduced the population of A. salmonicida faster than single suspensions and decreased the development of phage-resistant mutants. Because of this, they were proposed to be used to control furunculosis in aquaculture

 [122]
ETP-1
(Podoviridae)		 Multidrug resistant
Edwardsiella tarda 		Zebrafish
(Danio rerio)		 Edwardsiellosis

  • Isolation of a new phage from marine fish farm water in Jeju Island, Korea

  • Effective against multidrug-resistant E. tarda

  • When zebrafish was bath exposed for 12 days to phage ETP-1, and simultaneously challenged with E. tarda, the survival rate in phage-exposed fish was higher than that found in the control until 4 days post challenge

 [103]
ΦeiDWF, ΦeiAU, ΦeiMSLS
(Siphoviridae)		 Edwardsiella ictaluri Catfish Enteric septicemia

  • Isolation of new phages from geographically distant aquaculture ponds at different times

  • According to the genomic analysis, the phages are members of a lineage highly stable over time and geographic regions.

  • The genome analysis also revealed that the virus were virulent phages lacking lysogeny capacity, which will facilitate therapeutic applications

 [123]
FpV-1 to FpV-22:
FpV2, FpV4
(Podoviridae)
FpV7, FpV9, FpV10
(Siphoviridae)
FpV14, FpV19
(Myoviridae)		 Flavobacterium psychrophilum Rainbow trout
(Oncorhynchus mykiss) and other species of trouts		 Rainbow trout fry syndrome (RTFS) and bacterial coldwater disease (CWD)

  • Isolation of new phages from Danish rainbow trout farms, both with and without outbreaks of RTFS when the samples were taken

  • The phages showed a broad-host-range with a strong lytic potential against a large number of pathogenic F. psychrophilum host strains, indicating that they could have potential in the treatment of RTFS and CWD

 [124]
PFpW-3, PFpC-Y
(Myoviridae)
PFpW-6, PFpW-7
(Podoviridae)
PFpW-8
(Siphoviridae) 		Flavobacterium psychrophilum Ayu fish
(Plecoglossus altivelis altivelis)		 Systemic bacterial coldwater disease (CWD)

  • Isolation of new phages from ayu kidneys and pond water collected from Japanese ayu farms

  • Among the phages, in in vitro assays, PFpW-3 displayed high infectivity for F. psychrophilum isolated from ayu and from other fish, indicating that it could have interest for the treatment of CWD in Japanese ayu farms

 [125]
FCP1–FCP9
FCP1
(Podovariedae)		 Flavobacterium columnare Catfish
(Clarias batrachus)		 Columnaris disease

  • Isolation of new phages from the water and the bottom sediments of various geo-climatic regions of North India

  • When C. batrachus was treated with a virulent bacterial isolate and with phage FCP1 (applied via intramuscular, immersion, and oral), a significant decrease in host bacterium in sera, gill, liver, and kidney of challenged fishes was observed

  • Phage treatment resulted in disappearance of gross symptoms and 100% survival in experimentally infected C. batrachus

 [126]

Entries are grouped according to the pathogenic species, and the works related to the same species were ordered chronologically.