Phages as a Cohesive Prophylactic and Therapeutic Approach in Aquaculture Systems
Abstract
:1. Introduction
2. Bacterial Disease and Spoilage in the Fish and Seafood Industry
3. Phage Abundance and Significance in Aquatic Systems
Unfavorable Impact of Phages on Aquatic Reservoirs
4. Therapeutic Connotations of Phages in Aquacultures
4.1. Water Parameters
4.2. Multiplicity of Infection (MOI)
4.3. Fish Immunity
5. Phage Application in Fish and Seafood Industry in Practice
6. Discussion
Author Contributions
Funding
Conflicts of Interest
References
- FAO. The State of World Fisheries and Aquaculture 2020. Sustainability in Action. 2020. Available online: https://0-doi-org.brum.beds.ac.uk/10.4060/ca9229en (accessed on 1 July 2020).
- Overview of the Seafood Industry. Delaware Sea Grant, 2020. Available online: https://www.seafoodhealthfacts.org/seafood-choices/overview-seafood-industry (accessed on 1 July 2020).
- Swanson, D.; Block, R.; Mousa, S. Omega-3 Fatty Acids EPA and DHA: Health Benefits Throughout Life1. Adv. Nutr. 2012, 3, 1–7. [Google Scholar] [CrossRef]
- Whittle, P. Seafood Industry Struggling to Stay Afloat amid Outbreak. AP News. 2020. Available online: https://apnews.com/308352a4521171c83284a850bb892277 (accessed on 1 July 2020).
- Cabello, F.C.; Godfrey, H.P.; Tomova, A.; Ivanova, L.; Dölz, H.; Millanao, A.; Buschmann, A.H. Antimicrobial use in aquaculture re-examined: Its relevance to antimicrobial resistance and to animal and human health. Environ. Microbiol. 2013, 15, 1917–1942. [Google Scholar] [CrossRef]
- Endersen, L.; O’Mahony, J.; Hill, C.; Ross, R.P.; McAuliffe, O.; Coffey, A. Phage Therapy in the Food Industry. Annu. Rev. Food Sci. Technol. 2014, 5, 327–349. [Google Scholar] [CrossRef]
- Institute of Food Technologists. Antimicrobial Resistance: Implications for the Food System. An Expert Report, Funded by the IFT Foundation. Compr. Rev. Food Sci. Food Saf. 2006, 5, 71–137. [Google Scholar] [CrossRef]
- Liu, X.; Steele, J.C.; Meng, X.-Z. Usage, residue, and human health risk of antibiotics in Chinese aquaculture: A review. Environ. Pollut. 2017, 223, 161–169. [Google Scholar] [CrossRef]
- Richards, G.P. Bacteriophage remediation of bacterial pathogens in aquaculture: A review of the technology. Bacteriophage 2014, 4, e975540. [Google Scholar] [CrossRef] [Green Version]
- Yu, Y.-P.; Gong, T.; Jost, G.; Liu, W.-H.; Ye, D.-Z.; Luo, Z.-H. Isolation and characterization of five lytic bacteriophages infecting a Vibrio strain closely related to Vibrio owensii. FEMS Microbiol. Lett. 2013, 348, 112–119. [Google Scholar] [CrossRef] [Green Version]
- Chu, W.-H.; Zhu, W. Isolation of Bdellovibrio as Biological Therapeutic Agents Used For the Treatment of Aeromonas hydrophila Infection in Fish. Zoonoses Public Health 2009, 57, 258–264. [Google Scholar] [CrossRef]
- Kim, J.H.; Gomez, D.K.; Nakai, T.; Park, S.C. Isolation and identification of bacteriophages infecting ayu Plecoglossus altivelis altivelis specific Flavobacterium psychrophilum. Vet. Microbiol. 2010, 140, 109–115. [Google Scholar] [CrossRef]
- Jun, J.W.; Han, J.E.; Giri, S.S.; Tang, K.F.; Zhou, X.; Aranguren, L.F.; Kim, H.J.; Yun, S.; Chi, C.; Park, S.C. Phage Application for the Protection from Acute Hepatopancreatic Necrosis Disease (AHPND) in Penaeus vannamei. Indian J. Microbiol. 2017, 58, 114–117. [Google Scholar] [CrossRef]
- Stalin, N.; Srinivasan, P. Efficacy of potential phage cocktails against Vibrio harveyi and closely related Vibrio species isolated from shrimp aquaculture environment in the south east coast of India. Vet. Microbiol. 2017, 207, 83–96. [Google Scholar] [CrossRef] [PubMed]
- Patil, J.R.; Desai, S.N.; Roy, P.; Durgaiah, M.; Saravanan, R.S.; Vipra, A. Simulated hatchery system to assess bacteriophage efficacy against Vibrio harveyi. Dis. Aquat. Org. 2014, 112, 113–119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, Z.; Li, X.; Zhang, J.; Wang, X.; Wang, L.; Cao, Z.; Xu, Y. Use of phages to control Vibrio splendidus infection in the juvenile sea cucumber Apostichopus japonicus. Fish Shellfish Immunol. 2016, 54, 302–311. [Google Scholar] [CrossRef] [PubMed]
- Miranda, C.D.; Godoy, F.; Lee, M.R. Current Status of the Use of Antibiotics and the Antimicrobial Resistance in the Chilean Salmon Farms. Front. Microbiol. 2018, 9, 9. [Google Scholar] [CrossRef] [PubMed]
- Huss, H.H. FAO Fisheries Technical Paper—348; Food and Agriculture Organization of the United Nations: Rome, Italy, 1995; ISBN 92-5-103507-5. [Google Scholar]
- FAO. The State of World Fisheries and Aquaculture 2016: Contributing to Food Security and Nutrition for All; FAO: Rome, Italy, 2016; ISBN 978-92-5-109185-2. Available online: https://www.un-ilibrary.org/agriculture-rural-development-and-forestry/the-state-of-world-fisheries-and-aquaculture-2016_8e4e0ebf-en (accessed on 1 July 2020).
- Leung, T.L.F.; Bates, A.E. More rapid and severe disease outbreaks for aquaculture at the tropics: Implications for food security. J. Appl. Ecol. 2012, 50, 215–222. [Google Scholar] [CrossRef]
- Kalatzis, P.G.; Bastías, R.; Kokkari, C.; Katharios, P. Isolation and Characterization of Two Lytic Bacteriophages, φSt2 and φGrn1; Phage Therapy Application for Biological Control of Vibrio alginolyticus in Aquaculture Live Feeds. PLoS ONE 2016, 11, e0151101. [Google Scholar] [CrossRef] [Green Version]
- De Melo, A.G.; Levesque, S.; Moineau, S. Phages as friends and enemies in food processing. Curr. Opin. Biotechnol. 2018, 49, 185–190. [Google Scholar] [CrossRef]
- Komora, N.; Bruschi, C.; Ferreira, V.; Maciel, C.; Brandão, T.R.; Fernandes, R.; Saraiva, J.A.; Castro, S.M.; Teixeira, P. The protective effect of food matrices on Listeria lytic bacteriophage P100 application towards high pressure processing. Food Microbiol. 2018, 76, 416–425. [Google Scholar] [CrossRef]
- Żaczek, M.; Weber-Dąbrowska, B.; Górski, A. Phages in the global fruit and vegetable industry. J. Appl. Microbiol. 2014, 118, 537–556. [Google Scholar] [CrossRef]
- García, P.; Martinez, B.; Obeso, J.; Rodríguez, A. Bacteriophages and their application in food safety. Lett. Appl. Microbiol. 2008, 47, 479–485. [Google Scholar] [CrossRef]
- Kosznik-Kwaśnicka, K.; Topka, G.; Dydecka, A.; Necel, A.; Nejman-Faleńczyk, B.; Bloch, S.; Węgrzyn, G.; Węgrzyn, A. The Use of Bacteriophages in Animal Health and Food Protection. In Phage Therapy: A Practical Approach; Górski, A., Międzybrodzki, R., Borysowski, J., Eds.; Springer Science and Business Media LLC.: Berlin/Heidelberg, Germany, 2019; pp. 213–256. [Google Scholar]
- Strauch, E.; Hammerl, J.A.; Hertwig, S. Bacteriophages: New Tools for Safer Food? Rev. Chil. Infectol. 2015, 32, 678–688. [Google Scholar] [CrossRef]
- Katznelson, H. Bacteriophage in relation to plant diseases. Bot. Rev. 1937, 3, 499–521. [Google Scholar] [CrossRef]
- Miguéis, S.; Saraiva, C.; Esteves, A. Efficacy of LISTEX P100 at Different Concentrations for Reduction of Listeria monocytogenes Inoculated in Sashimi. J. Food Prot. 2017, 80, 2094–2098. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Soni, K.A.; Nannapaneni, R.; Hagens, S. Reduction of Listeria Monocytogenes on the Surface of Fresh Channel Catfish Fillets by Bacteriophage Listex P100. Foodborne Pathog. Dis. 2010, 7, 427–434. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, X.; Niu, Y.D.; Nan, Y.; Stanford, K.; Holley, R.; McAllister, T.A.; Narvaez-Bravo, C. SalmoFresh™ effectiveness in controlling Salmonella on romaine lettuce, mung bean sprouts and seeds. Int. J. Food Microbiol. 2019, 305, 108250. [Google Scholar] [CrossRef]
- Vikram, A.; Tokman, J.I.; Woolston, J.; Sulakvelidze, A. Phage Biocontrol Improves Food Safety by Significantly Reducing the Level and Prevalence of Escherichia coli O157:H7 in Various Foods. J. Food Prot. 2020, 83, 668–676. [Google Scholar] [CrossRef]
- Sudheesh, P.S.; Al-Ghabshi, A.; Al-Mazrooei, N.; Al-Habsi, S. Comparative Pathogenomics of Bacteria Causing Infectious Diseases in Fish. Int. J. Evol. Biol. 2012, 2012, 457264. [Google Scholar] [CrossRef]
- Rostami, H.; Abbaszadeh, S.; Shokri, S. Combined effects of lactoperoxidase system-whey protein coating and modified atmosphere packaging on the microbiological, chemical and sensory attributes of Pike-Perch fillets. J. Food Sci. Technol. 2017, 54, 3243–3250. [Google Scholar] [CrossRef]
- Erkmen, O.; Bozoglu, T.F. Spoilage of Fish and Other Seafoods. Chapter 18. In Food Microbiology: Principles into Practice; Erkmen, O., Bozoglu, T.F., Eds.; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2016; pp. 301–306. [Google Scholar] [CrossRef]
- Onarinde, B.A.; Dixon, R.A. Prospects for Biocontrol of Vibrio parahaemolyticus Contamination in Blue Mussels (Mytilus edulus)—A Year-Long Study. Front. Microbiol. 2018, 9, 9. [Google Scholar] [CrossRef]
- Kuley, E.; Durmuş, M.; Balikci, E.; Uçar, Y.; Regenstein, J.M.; Özogul, F. Fish spoilage bacterial growth and their biogenic amine accumulation: Inhibitory effects of olive by-products. Int. J. Food Prop. 2016, 20, 1029–1043. [Google Scholar] [CrossRef] [Green Version]
- Gram, L.; Huss, H.H. Microbiological spoilage of fish and fish products. Int. J. Food Microbiol. 1996, 33, 121–137. [Google Scholar] [CrossRef]
- Froelich, B.; Noble, R.T. Vibrio bacteria in raw oysters: Managing risks to human health. Philos. Trans. R. Soc. B Biol. Sci. 2016, 371, 20150209. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haq, S.M.; Dayal, H.H. Chronic Liver Disease and Consumption of Raw Oysters: A Potentially Lethal Combination—A Review of Vibrio vulnificus Septicemia. Am. J. Gastroenterol. 2005, 100, 1195–1199. [Google Scholar] [CrossRef] [PubMed]
- Austin, B.; Austin, D.A. Bacterial Fish Pathogens. Disease of Farmed and Wild Fish, 6th ed.; Springer: Berlin/Heidelberg, Germany, 2016. [Google Scholar] [CrossRef]
- Dwivedi, S.; Chauhan, P.S.; Mishra, S.; Kumar, A.; Singh, P.K.; Kamthan, M.; Chauhan, R.; Awasthi, S.; Yadav, S.; Mishra, A.; et al. Self-cleansing properties of Ganga during mass ritualistic bathing on Maha-Kumbh. Environ. Monit. Assess. 2020, 192, 221. [Google Scholar] [CrossRef]
- Weinbauer, M.G. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 2004, 28, 127–181. [Google Scholar] [CrossRef] [Green Version]
- Kavagutti, V.S.; Andrei, A.Ş.; Mehrshad, M.; Salcher, M.M.; Ghai, R. Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics. Microbiome 2019, 7, 1–15. [Google Scholar] [CrossRef] [Green Version]
- Breitbart, M. Marine Viruses: Truth or Dare. Annu. Rev. Mar. Sci. 2012, 4, 425–448. [Google Scholar] [CrossRef] [Green Version]
- Yu, Z.-C.; Chen, X.-L.; Shen, Q.-T.; Zhao, D.-L.; Tang, B.-L.; Su, H.-N.; Wu, Z.-Y.; Qin, Q.-L.; Xie, B.-B.; Zhang, X.-Y.; et al. Filamentous phages prevalent in Pseudoalteromonas spp. confer properties advantageous to host survival in Arctic sea ice. ISME J. 2015, 9, 871–881. [Google Scholar] [CrossRef] [Green Version]
- Weber-Dąbrowska, B.; Żaczek, M.; Dziedzic, B.; Łusiak-Szelachowska, M.; Kiejzik, M.; Górski, A.; Gworek, B.; Wierzbicki, K.; Eymontt, A. Bacteriophages in green biotechnology—The utilization of drinking water. In Industrial, Medical and Environmental Applications of Microorganisms: Current Status and Trends; Méndez-Vilas, A., Ed.; Wageningen Academic Publishers: Wageningen, The Netherlands, 2014; pp. 500–504. [Google Scholar]
- Adhya, S.; Merril, C. The road to phage therapy. Nature 2006, 443, 754–755. [Google Scholar] [CrossRef] [Green Version]
- Moon, K.; Kang, I.; Kim, S.; Kim, S.-J.; Cho, J.-C. Genomic and ecological study of two distinctive freshwater bacteriophages infecting a Comamonadaceae bacterium. Sci. Rep. 2018, 8, 7989. [Google Scholar] [CrossRef] [Green Version]
- Pourtois, J.; Tarnita, C.E.; Bonachela, J.A. Impact of Lytic Phages on Phosphorus- vs. Nitrogen-Limited Marine Microbes. Front. Microbiol. 2020, 11, 221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanmukh, S.; Khairnar, K.; Paunikar, W.; Lokhande, S. Understanding carbon regulation in aquatic systems—Bacteriophages as a model. F1000Research 2015, 4, 138. [Google Scholar] [CrossRef] [PubMed]
- Skov, P.V. CO2 in aquaculture. In The Cardiovascular System—Development, Plasticity and Physiological Responses; Elsevier BV: Amsterdam, The Netherlands, 2019; Volume 37, pp. 287–321. [Google Scholar]
- McMINN, B.R.; Korajkic, A.; Ashbolt, N. Evaluation ofBacteroides fragilis GB-124 bacteriophages as novel human-associated faecal indicators in the United States. Lett. Appl. Microbiol. 2014, 59, 115–121. [Google Scholar] [CrossRef] [PubMed]
- Blanch, A.R.; Lucena, F.; Muniesa, M.; Jofre, J. Fast and easy methods for the detection of coliphages. J. Microbiol. Methods 2020, 173, 105940. [Google Scholar] [CrossRef]
- Periasamy, D.; Sundaram, A. A novel approach for pathogen reduction in wastewater treatment. J. Environ. Health Sci. Eng. 2013, 11, 12. [Google Scholar] [CrossRef] [Green Version]
- Ghanem, N.; Kiesel, B.; Kallies, R.; Harms, H.; Chatzinotas, A.; Wick, L.Y. Marine Phages As Tracers: Effects of Size, Morphology, and Physico–Chemical Surface Properties on Transport in a Porous Medium. Environ. Sci. Technol. 2016, 50, 12816–12824. [Google Scholar] [CrossRef]
- Balcazar, J.L. How do bacteriophages promote antibiotic resistance in the environment? Clin. Microbiol. Infect. 2018, 24, 447–449. [Google Scholar] [CrossRef]
- Muniesa, M.; Colomer-Lluch, M.; Jofre, J. Potential impact of environmental bacteriophages in spreading antibiotic resistance genes. Future Microbiol. 2013, 8, 739–751. [Google Scholar] [CrossRef]
- Moon, K.; Jeon, J.H.; Kang, I.; Park, K.S.; Lee, K.; Cha, C.-J.; Lee, S.H.; Cho, J.-C. Freshwater viral metagenome reveals novel and functional phage-borne antibiotic resistance genes. Microbiome 2020, 8, 1–15. [Google Scholar] [CrossRef]
- Brown-Jaque, M.; Calero-Cáceres, W.; Muniesa, M. Transfer of antibiotic-resistance genes via phage-related mobile elements. Plasmid 2015, 79, 1–7. [Google Scholar] [CrossRef]
- Marti, E.; Variatza, E.; Balcázar, J.L. The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol. 2014, 22, 36–41. [Google Scholar] [CrossRef] [PubMed]
- Done, H.Y.; Venkatesan, A.K.; Halden, R.U. Does the Recent Growth of Aquaculture Create Antibiotic Resistance Threats Different from those Associated with Land Animal Production in Agriculture? AAPS J. 2015, 17, 513–524. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, C.; Zheng, L.; Zhou, J.; Zhao, H. Persistence and risk of antibiotic residues and antibiotic resistance genes in major mariculture sites in Southeast China. Sci. Total Environ. 2017, 580, 1175–1184. [Google Scholar] [CrossRef] [PubMed]
- Tekedar, H.C.; Kumru, S.; Blom, J.; Perkins, A.D.; Griffin, M.J.; Abdelhamed, H.; Karsi, A.; Lawrence, M.L. Comparative genomics of Aeromonas veronii: Identification of a pathotype impacting aquaculture globally. PLoS ONE 2019, 14, e0221018. [Google Scholar] [CrossRef] [Green Version]
- Petrovich, M.L.; Zilberman, A.; Kaplan, A.; Eliraz, G.R.; Wang, Y.; Langenfeld, K.; Duhaime, M.; Wigginton, K.; Poretsky, R.; Avisar, D.; et al. Microbial and Viral Communities and Their Antibiotic Resistance Genes Throughout a Hospital Wastewater Treatment System. Front. Microbiol. 2020, 11, 153. [Google Scholar] [CrossRef] [Green Version]
- Hoikkala, V.; Almeida, G.M.D.F.; Laanto, E.; Sundberg, L.-R. Aquaculture as a source of empirical evidence for coevolution between CRISPR-Cas and phage. Philos. Trans. R. Soc. B Biol. Sci. 2019, 374, 20180100. [Google Scholar] [CrossRef]
- Lin, D.M.; Koskella, B.; Lin, H.C. Phage therapy: An alternative to antibiotics in the age of multi-drug resistance. World J. Gastrointest. Pharm. 2017, 8, 162–173. [Google Scholar] [CrossRef]
- Middelboe, M.; Brussaard, C.P.D. Marine Viruses: Key Players in Marine Ecosystems. Viruses 2017, 9, 302. [Google Scholar] [CrossRef] [Green Version]
- Sharma, K.K.; Kalawat, U. Emerging Infections: Shewanella—A Series of Five Cases. J. Lab. Physicians 2010, 2, 61–65. [Google Scholar] [CrossRef]
- Batinovic, S.; Wassef, F.; Knowler, S.A.; Rice, D.T.F.; Stanton, C.R.; Rose, J.; Tucci, J.; Nittami, T.; Vinh, A.; Drummond, G.R.; et al. Bacteriophages in Natural and Artificial Environments. Pathogens 2019, 8, 100. [Google Scholar] [CrossRef] [Green Version]
- Allen, P.J.; Steeby, J.A. Aquaculture: Challenges and Promise. Nat. Educ. Knowl. 2011, 3, 12. [Google Scholar]
- Hites, R.A.; A Foran, J.; Carpenter, D.O.; Hamilton, M.C.; Knuth, B.A.; Schwager, S.J. Global Assessment of Organic Contaminants in Farmed Salmon. Science 2004, 303, 226–229. [Google Scholar] [CrossRef] [PubMed]
- Yates, M.V.; Gerba, C.P.; Kelley, L.M. Virus persistence in groundwater. Appl. Environ. Microbiol. 1985, 49, 778–781. [Google Scholar] [CrossRef] [Green Version]
- Jończyk-Matysiak, E.; Łodej, N.; Kula, D.; Owczarek, B.; Orwat, F.; Międzybrodzki, R.; Neuberg, J.; Bagińska, N.; Weber-Dąbrowska, B.; Górski, A. Factors determining phage stability/activity: Challenges in practical phage application. Expert Rev. Anti-Infect. 2019, 17, 583–606. [Google Scholar] [CrossRef]
- Jończyk, E.; Kłak, M.; Międzybrodzki, R.; Górski, A. The influence of external factors on bacteriophages—Review. Folia Microbiol. 2011, 56, 191–200. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.-W.; Kathariou, S. Temperature-Dependent Phage Resistance of Listeria monocytogenes Epidemic Clone II. Appl. Environ. Microbiol. 2009, 75, 2433–2438. [Google Scholar] [CrossRef] [Green Version]
- Groman, N.B.; Suzuki, G. Temperature and Lambda Phage Reproduction. J. Bacteriol. 1962, 84, 431–437. [Google Scholar] [CrossRef] [Green Version]
- Leon-Velarde, C.G.; Happonen, L.; Pajunen, M.I.; Leskinen, K.; Kropinski, A.M.; Mattinen, L.; Rajtor, M.; Zur, J.; Smith, D.; Chen, S.; et al. Yersinia enterocolitica-Specific Infection by Bacteriophages TG1 and ϕR1-RT Is Dependent on Temperature-Regulated Expression of the Phage Host Receptor OmpF. Appl. Environ. Microbiol. 2016, 82, 5340–5353. [Google Scholar] [CrossRef] [Green Version]
- Shan, J.; Korbsrisate, S.; Withatanung, P.; Adler, N.R.L.; Clokie, M.R.J.; Galyov, E.E. Temperature dependent bacteriophages of a tropical bacterial pathogen. Front. Microbiol. 2014, 5, 599. [Google Scholar] [CrossRef]
- Egilmez, H.I.; Morozov, A.; Clokie, M.R.J.; Shan, J.; Letarov, A.; Galyov, E.E. Temperature-dependent virus lifecycle choices may reveal and predict facets of the biology of opportunistic pathogenic bacteria. Sci. Rep. 2018, 8, 9642. [Google Scholar] [CrossRef] [Green Version]
- Madsen, L.; Bertelsen, S.K.; Dalsgaard, I.; Middelboe, M. Dispersal and Survival of Flavobacterium psychrophilum Phages In Vivo in Rainbow Trout and In Vitro under Laboratory Conditions: Implications for Their Use in Phage Therapy. Appl. Environ. Microbiol. 2013, 79, 4853–4861. [Google Scholar] [CrossRef] [Green Version]
- Akhwale, J.K.; Rohde, M.; Rohde, C.; Bunk, B.; Spröer, C.; Boga, H.I.; Klenk, H.-P.; Wittmann, J. Isolation, characterization and analysis of bacteriophages from the haloalkaline lake Elmenteita, Kenya. PLoS ONE 2019, 14, e0215734. [Google Scholar] [CrossRef] [Green Version]
- Silva, C.; Camilli, A. Niche adaptation limits bacteriophage predation of Vibrio cholerae in a nutrient-poor aquatic environment. Proc. Natl. Acad. Sci. USA 2019, 116, 1627–1632. [Google Scholar] [CrossRef] [Green Version]
- Bettarel, Y.; Desnues, A.; Rochelle-Newall, E. Lytic failure in cross-inoculationassays between phages and prokaryotes fromthree aquatic sites of contrasting salinity. FEMS Microbiol. Lett. 2010, 311, 113–118. [Google Scholar] [CrossRef]
- Choudhury, T.G.; Maiti, B.; Venugopal, M.N.; Karunasagar, I. Influence of some environmental variables and addition of r-lysozyme on efficacy of Vibrio harveyi phage for therapy. J. Biosci. 2019, 44, 8. [Google Scholar] [CrossRef]
- Muniesa, M.; Jofre, J. Factors influencing the replication of somatic coliphages in the water environment. Antonie Leeuwenhoek 2004, 86, 65–76. [Google Scholar] [CrossRef]
- Nilsson, E.; Li, K.; Fridlund, J.; Šulčius, S.; Bunse, C.; Karlsson, C.M.G.; Lindh, M.; Lundin, D.; Pinhassi, J.; Holmfeldt, K. Genomic and Seasonal Variations among Aquatic Phages Infecting the Baltic Sea Gammaproteobacterium Rheinheimera sp. Strain BAL341. Appl. Environ. Microbiol. 2019, 85, e01003-19. [Google Scholar] [CrossRef] [Green Version]
- Alonso-Sáez, L.; Morán, X.A.G.; Clokie, M.R. Low activity of lytic pelagiphages in coastal marine waters. ISME J. 2018, 12, 2100–2102. [Google Scholar] [CrossRef] [Green Version]
- Wierzbicki, K. (Ed.) Potencjalna Technologia Biologicznej Stabilizacji Mikrobiologii Wody Przeznaczonej do Spożycia; Institute of Technology and Life Sciences in Falenty: Warsaw, Poland, 2020; in press. (In Polish) [Google Scholar]
- Kim, J.H.; Choresca, C.H.; Shin, S.P.; Han, J.E.; Jun, J.W.; Park, S.C. Biological Control ofAeromonas salmonicidasubsp.salmonicidaInfection in Rainbow Trout (Oncorhynchus mykiss) UsingAeromonasPhage PAS-1. Transbound. Emerg. Dis. 2013, 62, 81–86. [Google Scholar] [CrossRef]
- Chen, L.; Yuan, S.; Liu, Q.; Mai, G.; Yang, J.; Deng, D.; Zhang, B.; Liu, C.; Ma, Y. In Vitro Design and Evaluation of Phage Cocktails Against Aeromonas salmonicida. Front. Microbiol. 2018, 9, 9. [Google Scholar] [CrossRef] [Green Version]
- Daniels, L.L.; Wais, A.C. Virulence in phage populations infecting Halobacterium cutirubrum. FEMS Microbiol. Ecol. 1998, 25, 129–134. [Google Scholar] [CrossRef]
- Almeida, G.M.D.F.; Mäkelä, K.; Laanto, E.; Pulkkinen, J.; Vielma, J.; Sundberg, L.-R. The Fate of Bacteriophages in Recirculating Aquaculture Systems (RAS)—Towards Developing Phage Therapy for RAS. Antibiotics 2019, 8, 192. [Google Scholar] [CrossRef] [Green Version]
- Soliman, W.S.; Shaapan, R.M.; Mohamed, L.A.; Gayed, S.S. Recent biocontrol measures for fish bacterial diseases, in particular to probiotics, bio-encapsulated vaccines, and phage therapy. Open Vet. J. 2019, 9, 190–195. [Google Scholar] [CrossRef] [Green Version]
- Międzybrodzki, R.; Borysowski, J.; Weber-Dąbrowska, B.; Fortuna, W.; Letkiewicz, S.; Szufnarowski, K.; Pawełczyk, Z.; Rogóż, P.; Kłak, M.; Wojtasik, E.; et al. Clinical Aspects of Phage Therapy. Adv. Appl. Microbiol. 2012, 83, 73–121. [Google Scholar]
- Łusiak-Szelachowska, M.; Żaczek, M.; Weber-Dąbrowska, B.; Międzybrodzki, R.; Kłak, M.; Fortuna, W.; Letkiewicz, S.; Rogóż, P.; Szufnarowski, K.; Jonczyk-Matysiak, E.; et al. Phage Neutralization by Sera of Patients Receiving Phage Therapy. Viral Immunol. 2014, 27, 295–304. [Google Scholar] [CrossRef] [Green Version]
- Żaczek, M.; Łusiak-Szelachowska, M.; Weber-Dąbrowska, B.; Międzybrodzki, R.; Fortuna, W.; Rogóż, P.; Letkiewicz, S.; Górski, A. Humoral Immune Response to Phage-Based Therapeutics. In Phage Therapy: A Practical Approach; Górski, A., Międzybrodzki, R., Borysowski, J., Eds.; Springer Science and Business Media LLC.: Berlin/Heidelberg, Germany, 2019; pp. 123–143. [Google Scholar]
- Żaczek, M.; Łusiak-Szelachowska, M.; Jończyk-Matysiak, E.; Weber-Dąbrowska, B.; Międzybrodzki, R.; Owczarek, B.; Kopciuch, A.; Fortuna, W.; Rogóż, P.; Górski, A. Antibody Production in Response to Staphylococcal MS-1 Phage Cocktail in Patients Undergoing Phage Therapy. Front. Microbiol. 2016, 7, 1681. [Google Scholar] [CrossRef] [Green Version]
- Górski, A.; Dąbrowska, K.; Międzybrodzki, R.; Weber-Dąbrowska, B.; Łusiak-Szelachowska, M.; Jończyk-Matysiak, E.; Borysowski, J. Phages and immunomodulation. Future Microbiol. 2017, 12, 905–914. [Google Scholar] [CrossRef] [Green Version]
- Górski, A.; Międzybrodzki, R.; Jończyk-Matysiak, E.; Żaczek, M.; Borysowski, J. Phage-specific diverse effects of bacterial viruses on the immune system. Future Microbiol. 2019, 14, 1171–1174. [Google Scholar] [CrossRef] [Green Version]
- Silva, Y.J.; Moreirinha, C.; Pereira, C.; Costa, L.; Rocha, R.J.M.; Cunha, Â.; Gomes, N.; Calado, R.; Almeida, M.A. Biological control of Aeromonas salmonicida infection in juvenile Senegalese sole (Solea senegalensis) with Phage AS-A. Aquaculture 2016, 450, 225–233. [Google Scholar] [CrossRef] [Green Version]
- He, Y.; Yang, H. The gastrointestinal phage communities of the cultivated freshwater fishes. FEMS Microbiol. Lett. 2014, 362, 027. [Google Scholar] [CrossRef]
- Almeida, G.M.D.F.; Laanto, E.; Ashrafi, R.; Sundberg, L.-R. Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria. MBio 2019, 10, 01984-19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silveira, C.B.; Rohwer, F. Piggyback-the-Winner in host-associated microbial communities. npj Biofilms Microbiomes 2016, 2, 16010. [Google Scholar] [CrossRef] [PubMed]
- Barr, J.J.; Auro, R.; Sam-Soon, N.; Kassegne, S.; Peters, G.; Bonilla, N.; Hatay, M.; Mourtada, S.; Bailey, B.; Youle, M.; et al. Subdiffusive motion of bacteriophage in mucosal surfaces increases the frequency of bacterial encounters. Proc. Natl. Acad. Sci. USA 2015, 112, 13675–13680. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schulz, P.; Pajdak, J.; Robak, S.; Dastych, J.; Siwicki, A.K. Bacteriophage-based cocktail modulates selected immunological parameters and post-challenge survival of rainbow trout (Oncorhynchus mykiss). J. Fish Dis. 2019, 42, 1151–1160. [Google Scholar] [CrossRef]
- Schulz, P.; Robak, S.; Dastych, J.; Siwicki, A.K. Influence of bacteriophages cocktail on European eel (Anguilla anguilla) immunity and survival after experimental challenge. Fish Shellfish Immunol. 2019, 84, 28–37. [Google Scholar] [CrossRef]
- Yun, S.; Jun, J.W.; Giri, S.S.; Kim, H.J.; Chi, C.; Kim, S.G.; Kim, S.W.; Kang, J.W.; Han, S.J.; Kwon, J.; et al. Immunostimulation of Cyprinus carpio using phage lysate of Aeromonas hydrophila. Fish Shellfish Immunol. 2019, 86, 680–687. [Google Scholar] [CrossRef]
- Laanto, E.; Bamford, J.K.H.; Laakso, J.; Sundberg, L.-R. Phage-Driven Loss of Virulence in a Fish Pathogenic Bacterium. PLoS ONE 2012, 7, e53157. [Google Scholar] [CrossRef] [Green Version]
- Holmfeldt, K.; Middelboe, M.; Nybroe, O.; Riemann, L. Large Variabilities in Host Strain Susceptibility and Phage Host Range Govern Interactions between Lytic Marine Phages and Their Flavobacterium Hosts. Appl. Environ. Microbiol. 2007, 73, 6730–6739. [Google Scholar] [CrossRef] [Green Version]
- Luo, L.; Liao, G.; Liu, C.; Jiang, X.; Lin, M.; Zhao, C.; Tao, J.; Huang, Z. Characterization of bacteriophage HN48 and its protective effects in Nile tilapia Oreochromis niloticus against Streptococcus agalactiae infections. J. Fish Dis. 2018, 41, 1477–1484. [Google Scholar] [CrossRef]
- Akmal, M.; Rahimi-Midani, A.; Hafeez-Ur-Rehman, M.; Hussain, A.; Choi, T.-J. Isolation, Characterization, and Application of a Bacteriophage Infecting the Fish Pathogen Aeromonas hydrophila. Pathogens 2020, 9, 215. [Google Scholar] [CrossRef] [Green Version]
- Rørbo, N.; Rønneseth, A.; Kalatzis, P.G.; Rasmussen, B.B.; Engell-Sørensen, K.; Kleppen, H.P.; Wergeland, H.I.; Gram, L.; Middelboe, M. Exploring the Effect of Phage Therapy in Preventing Vibrio anguillarum Infections in Cod and Turbot Larvae. Antibiotics 2018, 7, 42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.; Fan, J.; Yan, T.; Liu, Q.; Yuan, S.; Zhang, H.; Yang, J.; Deng, D.; Huang, S.; Ma, Y. Isolation and Characterization of Specific Phages to Prepare a Cocktail Preventing Vibrio sp. Va-F3 Infections in Shrimp (Litopenaeus vannamei). Front. Microbiol. 2019, 10, 2337. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Castillo, D.; Higuera, G.; Villa, M.; Middelboe, M.; Dalsgaard, I.; Madsen, L.; Espejo, R. Diversity of Flavobacterium psychrophilum and the potential use of its phages for protection against bacterial cold water disease in salmonids. J. Fish Dis. 2012, 35, 193–201. [Google Scholar] [CrossRef] [PubMed]
- Jun, J.W.; Kim, H.J.; Kil Yun, S.; Chai, J.Y.; Park, S.C. Eating oysters without risk of vibriosis: Application of a bacteriophage against Vibrio parahaemolyticus in oysters. Int. J. Food Microbiol. 2014, 188, 31–35. [Google Scholar] [CrossRef]
- Pirnay, J.-P.; De Vos, D.; Verbeken, G. Clinical application of bacteriophages in Europe. Microbiol. Aust. 2019, 40, 8. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Li, L.; Zhao, Z.; Peng, D.; Zhou, X. Polar flagella rotation in Vibrio parahaemolyticus confers resistance to bacteriophage infection. Sci. Rep. 2016, 6, 26147. [Google Scholar] [CrossRef]
- Hai, N. The use of probiotics in aquaculture. J. Appl. Microbiol. 2015, 119, 917–935. [Google Scholar] [CrossRef]
- Nakai, T.; Park, S.C. Bacteriophage therapy of infectious diseases in aquaculture. Res. Microbiol. 2002, 153, 13–18. [Google Scholar] [CrossRef]
- The Seventh Framework Programme—AQUAPHAGE. Available online: https://cordis.europa.eu/project/id/269175 (accessed on 1 July 2020).
Gram-Negative | Gram-Positive |
---|---|
Escherichia | Bacillus |
Serratia | Clostridium |
Morganella | Lactobacillus |
Vibrio1 | Corynebacterium |
Photobacterium1,3 | Streptococcus6 |
Aeromonas2 | Renibacterium7 |
Proteus4 | Mycobacteria * |
Alcaligenes5 | |
Enterobacter4 | |
Pseudomonas | |
Moraxella | |
Acinetobacter5 | |
Shewanella putrefaciens5 | |
Flavobacterium5 | |
Raoultella | |
Edwarsiella | |
Yersinia |
Target Bacteria | Fish or Seafood Species | Method of Application | Outcome | Reference (Year) |
---|---|---|---|---|
Vibrio parahaemolyticus | Blue mussels (Mytilus edulus) | 2.5-L glass beakers positioned at 4 °C with 8–16 infected (109 cfu/mL) mussels and approx. 0.1 × 106 pfu of phage cocktail (12 phages) added prior to experiment | Phage cocktail was effective in significantly reducing V. parahaemolyticus to undetectable numbers in mussels | [36] (2018) |
Vibrio parahaemolyticus | Shrimp (Penaeus vannamei) | Infected (5.0 × 105 cfu/mL) juvenile shrimps were fed with pellets containing the phage (1.5 × 108 pfu/shrimp) or immersed in phage suspension (1.5 × 106 pfu/mL) 1 h after the bacterial challenge or prior to infection | Mortality in groups treated 1 h after bacterial infection was 100%; prophylactic use of phages resulted in mortality varied from 25% to 50% | [13] (2017) |
Streptococcus agalactiae | Nile tilapia (Oreochromis niloticus) | Single phage preparation added to fish tanks | Treated fish had 60% survival rates and a delayed mean death time of about three days when compared to the control group | [111] (2018) |
Aeromonas hydrophila | Loach (Misgurnus anguillicaudatus) | Infected (1 × 107 cfu/mL) loah treated by immersion in water containing 1.0 × 108 pfu/mL of single phage preparation | Mortality rates were 16%, 53%, 57%, and 56.67% after 24, 48, 72, 96 h respectively when compared to the control group with 100% mortality; most of the surviving fish showed no disease symptoms | [112] (2020) |
Vibrio anguillarum | Atlantic cod (Gadus morhua) | Infected (0.5–1 × 106 cfu/mL) fish eggs were incubated at 5.5 °C (Atlantic cod) and 15.5 °C (turbot) in 24-well plates with 2 mL sterile and oxygenated seawater with addition of single phage preparation to a final concentration of 0.5–8 × 108 pfu/mL | The maximum reduction in mortality varied from 29% to 92% for turbot and from 49% to 86% for Atlantic cod assessed during the experiment and depending on the strain used; notably, reduction in mortality was not significant in the majority of cases at the end of the experiment | [113] (2018) |
Vibrio sp. VA-F3 | Shrimp (Litopenaeus vannamei) | 30 infected (2 × 106 cfu/mL) shrimps received the treatment of phage cocktail (5 phages) at 2 × 107 pfu/mL | Survival rate assessed after seven days of cultivation reached 91.4% when compared to 20% rate in the untreated control group | [114] (2019) |
Flavobacterium psychrophilum | Salmo salar, Oncorhynchus mykiss | Fish were infected by intraperitoneal injection of bacteria and single phage mixture at MOI = 10 pfu/cfu and were kept at 15 °C for 15 days | Percentage mortality reduction in the presence of the phage varied from 16% to 100% | [115] (2012) |
Vibrio splendidus | Sea cucumber (Apostichopus japonicus) | Diet supplemented with three phages alone or as a cocktail was implemented for 60 days before immersion in seawater with 6 × 106 cfu/mL of bacterial pathogen | Survival rate during the next ten days was 18% for the control group, 82% for the phage cocktail, and 65%, 58%, 50% for the three phages applied alone | [16] (2016) |
Vibrio harveyi | Black tiger shrimp (Litopenaeus monodon) | Shrimp postlarvae (PL2 stage) were acclimated for three days in 1.25-L glass flasks. Next, 1010 pfu/mL single phage were added and 30 min later 107 cfu/mL V. harveyi | After 10 days, mortality in the treated group was 20% when compared to >70% in tanks challenged only with V. harveyi | [15] (2014) |
Vibrio parahaemolyticus | Oysters | Oysters infected with multidrug-resistant pandemic strain were immersed in solution containing single phage | After 72 h bacterial growth reduction was from 8.9 × 106 cfu/mL (control group) to 1.94 cfu/mL (treatment group) | [116] (2014) |
Aeromonas salmonicida subsp. salmonicida | Rainbow trout (Oncorhynchus mykiss) | 3–4-month rainbow trout were kept in aerated 50 L glass tanks (20 fish/tank). Fish were intramuscularly injected with 2.5 × 102 cfu/fish and with single phage at MOI = 10,000 immediately after the bacterial challenge; fish were observed for 14 days | Fish in the treated group showed a 26.7% survival rate; the surviving fish did not show ulcerative lesions and remained healthy until 14 days postadministration; all fish from the control group died | [90] (2012) |
Aeromonas salmonicida | Senegalese sole (Solea senegalensis) | Infected Senegalese sole juveniles were treated with single phage preparation | After 72 h, infected fish juveniles treated with phages showed no mortality contrary to 36% mortality in the control group | [101] (2016) |
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Żaczek, M.; Weber-Dąbrowska, B.; Górski, A. Phages as a Cohesive Prophylactic and Therapeutic Approach in Aquaculture Systems. Antibiotics 2020, 9, 564. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics9090564
Żaczek M, Weber-Dąbrowska B, Górski A. Phages as a Cohesive Prophylactic and Therapeutic Approach in Aquaculture Systems. Antibiotics. 2020; 9(9):564. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics9090564
Chicago/Turabian StyleŻaczek, Maciej, Beata Weber-Dąbrowska, and Andrzej Górski. 2020. "Phages as a Cohesive Prophylactic and Therapeutic Approach in Aquaculture Systems" Antibiotics 9, no. 9: 564. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics9090564