Desmecht, Salomé ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI)
Antoine, Céline ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Touzain, Fabrice
Oberlé, Kenny
Calvez, Ségolène
Laforêt, Fanny
Vermeersch, Marjorie
Le Roux, Aurélie
Schonbrodt, Alain
Lieffrig, François ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Immunologie et vaccinologie
Thiry, Damien ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Bactériologie vétérinaire et maladies bactériennes animales
Language :
English
Title :
Characterization and in vivo efficacy in the Galleria mellonella model of novel bacteriophages targeting Aeromonas salmonicida
Ackermann, H.W., 5500 Phages examined in the electron microscope. Arch. Virol. 152 (2007), 227–243, 10.1007/s00705-006-0849-1.
Adamczuk, M., Dziewit, L., Genome-based insights into the resistome and mobilome of multidrug-resistant Aeromonas sp. ARM81 isolated from wastewater. Arch. Microbiol. 199 (2017), 177–183, 10.1007/s00203-016-1285-6.
Alcock, B.P., Huynh, W., Chalil, R., Smith, K.W., Raphenya, A.R., Wlodarski, M.A., Edalatmand, A., Petkau, A., Syed, S.A., Tsang, K.K., Baker, S.J.C., Dave, M., Mccarthy, M.C., Mukiri, K.M., Nasir, J.A., Golbon, B., Imtiaz, H., Jiang, X., Kaur, K., Kwong, M., Liang, Z.C., Niu, K.C., Shan, P., Yang, J.Y.J., Gray, K.L., Hoad, G.R., Jia, B., Bhando, T., Carfrae, L.A., Farha, M.A., French, S., Gordzevich, R., Rachwalski, K., Tu, M.M., Bordeleau, E., Dooley, D., Griffiths, E., Zubyk, H.L., Brown, E.D., Maguire, F., Beiko, R.G., Hsiao, W.W.L., Brinkman, F.S.L., Van Domselaar, G., Mcarthur, A.G., CARD 2023: expanded curation, support for machine learning, and resistome prediction at the Comprehensive Antibiotic Resistance Database. Nucleic Acids Res. 51 (2023), D690–D699, 10.1093/nar/gkac920.
Antoine, C., Laforêt, F., Blasdel, B., Fall, A., Duprez, J.-N., Mainil, J., Delcenserie, V., Thiry, D., In Vitro characterization and in vivo efficacy assessment in Galleria mellonella larvae of newly isolated bacteriophages against Escherichia coli K1. Viruses, 13, 2021, 2005, 10.3390/v13102005.
Bacchetti De Gregoris, T., Aldred, N., Clare, A.S., Burgess, J.G., Improvement of phylum- and class-specific primers for real-time PCR quantification of bacterial taxa. J. Microbiol. Methods 86 (2011), 351–356, 10.1016/j.mimet.2011.06.010.
Bailly-Bechet, M., Vergassola, M., Rocha, E., Causes for the intriguing presence of tRNAs in phages. Genome Res. 17 (2007), 1486–1495, 10.1101/GR.6649807.
Berg, A., Rødseth, O.M., Hansen, T., Fish size at vaccination influence the development of side-effects in Atlantic salmon (Salmo Salar L.). Aquaculture 265 (2007), 9–15, 10.1016/J.AQUACULTURE.2007.02.014.
Bobate, S., Mahalle, S., Dafale, N.A., Bajaj, A., Emergence of environmental antibiotic resistance: Mechanism, monitoring and management. Environ. Adv., 13, 2023, 100409, 10.1016/j.envadv.2023.100409.
Boone, D.R., Castenholz, R.W., Garrity, G.M., Bergey's Manual® of Systematic Bacteriology. second ed, 2001, Springer, New York.
Bouras, G., Nepal, R., Houtak, G., Psaltis, A.J., Wormald, P.J., Vreugde, S., Pharokka: a fast scalable bacteriophage annotation tool. Bioinf. (Oxf.), 39, 2023, btac776, 10.1093/bioinformatics/btac776.
Bouras, G., Grigson, S.R., Mirdita, M., Heinzinger, M., Papudeshi, B., Mallawaarachchi, V., Green, R., Kim, R.S., Mihalia, V., Psaltis, A.J., Wormald, P.J., Vreugde, S., Steinegger, M., Edwards, R.A., Protein structure-informed bacteriophage genome annotation with Phold. Nucleic Acids Res., 54, 2026, gkaf1448, 10.1093/nar/gkaf1448.
Chart, H., Shaw, D.H., Ishiguro, E.E., Trust, T.J., Structural and immunochemical homogeneity of Aeromonas salmonicida lipopolysaccharide. J. Bacteriol., 158, 1984, 16, 10.1128/JB.158.1.16-22.1984.
Cheng, Y., Gao, D., Xia, Y., Wang, Z., Bai, M., Luo, K., Cui, X., Wang, Y., Zhang, S., Xiao, W., Characterization of novel bacteriophage AhyVDH1 and its lytic activity against Aeromonas hydrophila. Curr. Microbiol. 78 (2021), 329–337, 10.1007/S00284-020-02279-7.
Chu, S., Noonan, B., Cavaignac, S., Trust, T.J., Endogenous mutagenesis by an insertion sequence element identifies Aeromonas salmonicida AbcA as an ATP-binding cassette transport protein required for biogenesis of smooth lipopolysaccharide. Proc. Natl. Acad. Sci. USA 92 (1995), 5754–5758, 10.1073/PNAS.92.12.5754.
Culot, A., Grosset, N., Gautier, M., Overcoming the challenges of phage therapy for industrial aquaculture: A review. Aquaculture, 513, 2019, 734423, 10.1016/j.aquaculture.2019.734423.
Cutuli, M.A., Petronio Petronio, G., Vergalito, F., Magnifico, I., Pietrangelo, L., Venditti, N., Di Marco, R., Galleria mellonella as a consolidated in vivo model hosts: New developments in antibacterial strategies and novel drug testing. Virulence, 10, 2019, 527, 10.1080/21505594.2019.1621649.
Daher, R.K., Filion, G., Tan, S.G.E., Dallaire-Dufresne, S., Paquet, V.E., Charette, S.J., Alteration of virulence factors and rearrangement of pAsa5 plasmid caused by the growth of Aeromonas salmonicida in stressful conditions. Vet. Microbiol. 152 (2011), 353–360, 10.1016/J.VETMIC.2011.04.034.
Dallaire-Dufresne, S., Tanaka, K.H., Trudel, M.V., Lafaille, A., Charette, S.J., Virulence, genomic features, and plasticity of Aeromonas salmonicida subsp. salmonicida, the causative agent of fish furunculosis. Vet. Microbiol. 169 (2014), 1–7, 10.1016/j.vetmic.2013.06.025.
Desbois, A.P., Coote, P.J., Utility of greater wax moth larva (Galleria mellonella) for evaluating the toxicity and efficacy of new antimicrobial agents. Advances in Applied Microbiology, 2012, Academic Press Inc., 25–53, 10.1016/B978-0-12-394805-2.00002-6.
Desmecht, S., Touzain, F., Olivier, T., Antoine, C., Beven, V., Meex, C., Lieffrig, F., Charette, S.J., Thiry, D., Genomic and virulence insights of Western European Aeromonas salmonicida subsp. salmonicida and development of Galleria mellonella infection assay. J. Appl. Microbiol., 136, 2025, lxaf193, 10.1093/jambio/lxaf193.
Duneau, D., Ferdy, J.B., Revah, J., Kondolf, H., Ortiz, G.A., Lazzaro, B.P., Buchon, N., Stochastic variation in the initial phase of bacterial infection predicts the probability of survival in D. melanogaster. eLife, 6, 2017, e28298, 10.7554/eLife.28298.
Dunne, M., Rupf, B., Tala, M., Qabrati, X., Ernst, P., Shen, Y., Sumrall, E., Heeb, L., Plückthun, A., Loessner, M.J., Kilcher, S., Reprogramming bacteriophage host range through structure-guided design of chimeric receptor binding proteins. Cell Rep. 29 (2019), 1336–1350.e4, 10.1016/J.CELREP.2019.09.062.
Ebanks, R.O., Goguen, M., McKinnon, S., Pinto, D.M., Ross, N.W., Identification of the major outer membrane proteins of Aeromonas salmonicida. Dis. Aquat. Org. 68 (2005), 29–38, 10.3354/DAO068029.
European Medicines Agency, Authorised fish products: situation in Europe (EMA/CMDv/650880/2018 rev 4) [Excel spreadsheet]. 2022, European Medicines Agency, Amsterdam.
European Parliament and Council, Regulation (EU) 2019/6 of the European Parliament and of the Council on veterinary medicinal products (Article 107, OJ L 4, 7.1.2022). https://eur-lex.europa.eu/eli/reg/2019/6/2022-01-28/eng, 2019 (accessed 28 January 2026).
Froquet, R., Cherix, N., Burr, S.E., Frey, J., Vilches, S., Tomas, J.M., Cosson, P., Alternative host model to evaluate Aeromonas virulence. Appl. Environ. Microbiol. 73 (2007), 5657–5659, 10.1128/AEM.00908-07.
Garduño, R.A., Moore, A.R., Olivier, G., Lizama, A.L., Garduño, E., Kay, W.W., Host cell invasion and intracellular residence by Aeromonas salmonicida: Role of the S-layer. Can. J. Microbiol. 46 (2000), 660–668, 10.1139/w00-034.
Ghugare, G.S., Nimkande, V.D., Khairnar, K., Isolation and enrichment of bacteriophages by membrane filtration immobilization technique. Curr. Protoc. Cell Biol., 79, 2018, e41, 10.1002/CPCB.41.
Gonzalez-Menendez, E., Fernandez, L., Gutierrez, D., Rodríguez, A., Martínez, B., GarcíaI, P., Comparative analysis of different preservation techniques for the storage of Staphylococcus phages aimed for the industrial development of phage-based antimicrobial products. PLoS One, 13, 2018, e020572, 10.1371/JOURNAL.PONE.0205728.
Gurevich, A., Saveliev, V., Vyahhi, N., Tesler, G., QUAST: Quality assessment tool for genome assemblies. Bioinformatics 29 (2013), 1072–1075, 10.1093/bioinformatics/btt086.
Gustafson, C.E., Chu, S., Trust, T.J., Mutagenesis of the paracrystalline surface protein array of Aeromonas salmonicida by endogenous insertion elements. J. Mol. Biol. 237 (1994), 452–463, 10.1006/JMBI.1994.1247.
Heller, K.J., Molecular interaction between bacteriophage and the gram-negative cell envelope. Arch. Microbiol. 158 (1992), 235–248, 10.1007/BF00245239.
Hua, J., Huet, A., Lopez, C.A., Toropova, K., Pope, W.H., Duda, R.L., Hendrix, R.W., Conway, J.F., Capsids and genomes of jumbo-sized bacteriophages reveal the evolutionary reach of the HK97 fold. mBio, 8, 2017, e01579–17, 10.1128/mBio.01579-17.
Imbeault, S., Parent, S., Lagacé, M., Uhland, C.F., Blais, J.F., Using bacteriophages to prevent furunculosis caused by Aeromonas salmonicida in farmed brook trout. J. Aquat. Anim. Health 18 (2006), 203–214, 10.1577/H06-019.1.
Ishiguro, E.E., Kay, W.W., Ainsworth, T., Chamberlain, J.B., Austen, R.A., Buckley, J.T., Trust, T.J., Loss of virulence during culture of Aeromonas salmonicida at high temperature. J. Bacteriol. 148 (1981), 333–340.
Ishiguro, E.E., Ainsworth, T., Harkness, R.E., Kay, W.W., Trust, T.J., A temperate bacteriophage specific for strains of Aeromonas salmonicida possessing A-layer, a cell surface virulence factor. Curr. Microbiol. 10 (1984), 199–202.
Keeling, S.E., Brosnahan, C.L., Johnston, C., Wallis, R., Gudkovs, N., McDonald, W.L., Development and validation of a real-time PCR assay for the detection of Aeromonas salmonicida. J. Fish Dis. 36 (2013), 495–503, 10.1111/jfd.12014.
Kim, J.H., Choresca, C.H., Shin, S.P., Han, J.E., Jun, J.W., Park, S.C., Biological control of Aeromonas salmonicida subsp. salmonicida infection in rainbow trout (Oncorhynchus mykiss) using Aeromonas phage PAS-1. Transbound. Emerg. Dis. 62 (2015), 81–86, 10.1111/tbed.12088.
Koppang, E.O., Haugarvoll, E., Hordvik, I., Aune, L., Poppe, T.T., Vaccine-associated granulomatous inflammation and melanin accumulation in Atlantic salmon, Salmo salar L., white muscle. J. Fish Dis. 28 (2005), 13–22, 10.1111/J.1365-2761.2004.00583.X.
Kowalska, J.D., Kazimierczak, J., Sowińska, P.M., Wójcik, E.A., Siwicki, A.K., Dastych, J., Growing trend of fighting infections in aquaculture environment—Opportunities and challenges of phage therapy. Antibiotics 9 (2020), 1–17, 10.3390/antibiotics9060301.
Kumari, R., Yadav, R., Kumar, D., Chaube, R., Nath, G., Evaluation of bacteriophage therapy of Aeromonas hydrophila infection in a freshwater fish, Pangasius buchanani. Front. Aquac., 2, 2023, e1201466, 10.3389/faquc.2023.1201466.
Laforêt, F., Antoine, C., Reuter, B.B., Detilleux, J., Pirnay, J.P., Brisse, S., Fall, A., Duprez, J.N., Delcenserie, V., Thiry, D., In vitro and in vivo assessments of two newly isolated bacteriophages against an ST13 urinary tract infection Klebsiella pneumoniae. Viruses, 14, 2022, 1079, 10.3390/V14051079.
Landry, E.F., Zsigray, R.M., Effects of calcium on the lytic cycle of Bacillus subtilis phage 41c. J. Gen. Virol. 51 (1980), 125–135, 10.1099/0022-1317-51-1-125.
Le Bouquin, S., Thomas, R., Jamin, M., Baron, S., Hanne-Poujade, S., Chauvin, C., A baseline survey of antimicrobial use and health issues in the freshwater salmonid industry in France. Aquacult. Rep., 21, 2021, 100906, 10.1016/j.aqrep.2021.100906.
Lillehaug, A., Lunder, T., Poppe, T.T., Field testing of adjuvanted furunculosis vaccines in Atlantic salmon, Salmo salar L. J. Fish Dis. 15 (1992), 485–496, 10.1111/J.1365-2761.1992.TB00680.X.
Liu, B., Zheng, D., Zhou, S., Chen, L., Yang, J., VFDB 2022: a general classification scheme for bacterial virulence factors. Nucleic Acids Res. 50 (2022), D912–D917, 10.1093/NAR/GKAB1107.
Magiorakos, A.-P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M.E., Giske, C.G., Harbarth, S., Hindler, J.F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D.L., Rice, L.B., Stelling, J., Struelens, M.J., Vatopoulos, A., Weber, J.T., Monnet, D.L., Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18 (2012), 268–281, 10.1111/j.1469-0691.2011.03570.x.
Menanteau-Ledouble, S., Kumar, G., Saleh, M., El-Matbouli, M., Aeromonas salmonicida: updates on an old acquaintance. Dis. Aquat. Org. 120 (2016), 49–68, 10.3354/DAO03006.
Ménard, G., Rouillon, A., Cattoir, V., Donnio, P.Y., Galleria mellonella as a suitable model of bacterial infection: Past, present and future. Front. Cell. Infect. Microbiol., 11, 2021, 782733, 10.3389/fcimb.2021.782733.
Midtlyng, P.J., Vaccination against furunculosis. Gudding, R., Lillehaug, A., Evensen, Ø., (eds.) Fish Vaccination, first ed., 2014, 185–199, 10.1002/9781118806913.CH16.
Mo, J., Kleppen, H.P., Frantzen, C., Bårdsen, E., Støtvig, I., Gillund, B., Use of the bacteriophage product Custus®YRS for infection pressure control and disease prevention in Atlantic salmon. Norwegian. Vet. J. 3 (2023), M–198 https://nvt.vetnett.no/journal/2023/3/m-198/Bruk_av_bakteriofagproduktet_Custus%C2%AEYRS_til_smittepresskontroll_og_sykdomsforebygging_hos_atlantisk_laks.
Munn, C.B., Ishiguro, E.E., Kay, W.W., Trust, T.J., Role of surface components in serum resistance of virulent Aeromonas salmonicida. Infect. Immun. 36 (1982), 1069–1075, 10.1128/IAI.36.3.1069-1075.1982.
Navez, M., Antoine, C., Laforêt, F., Goya-Jorge, E., Douny, C., Scippo, M.-L., Vermeersch, M., Duprez, J.-N., Daube, G., Mainil, J., Taminiau, B., Delcenserie, V., Thiry, D., In vitro effect on piglet gut microbiota and in vivo assessment of newly isolated bacteriophages against F18 Enterotoxigenic Escherichia coli (ETEC). Viruses, 15, 2023, 1053, 10.3390/V15051053.
Nayak, S.K., Current prospects and challenges in fish vaccine development in India with special reference to Aeromonas hydrophila vaccine. Fish Shellfish Immunol. 100 (2020), 283–299, 10.1016/j.fsi.2020.01.064.
Ngassam-Tchamba, C., Duprez, J.N., Fergestad, M., De Visscher, A., L'Abee-Lund, T., De Vliegher, S., Wasteson, Y., Touzain, F., Blanchard, Y., Lavigne, R., Chanishvili, N., Cassart, D., Mainil, J., Thiry, D., In vitro and in vivo assessment of phage therapy against Staphylococcus aureus causing bovine mastitis. J Glob Antimicrob Resist 22 (2020), 762–770, 10.1016/J.JGAR.2020.06.020.
Nishimura, Y., Yoshida, T., Kuronishi, M., Uehara, H., Ogata, H., Goto, S., ViPTree: The viral proteomic tree server. Bioinformatics 33 (2017), 2379–2380, 10.1093/bioinformatics/btx157.
Olson, R.D., Assaf, R., Brettin, T., Conrad, N., Cucinell, C., Davis, J.J., Dempsey, D.M., Dickerman, A., Dietrich, E.M., Kenyon, R.W., Kuscuoglu, M., Lefkowitz, E.J., Lu, J., Machi, D., Macken, C., Mao, C., Niewiadomska, A., Nguyen, M., Olsen, G.J., Overbeek, J.C., Parrello, B., Parrello, V., Porter, J.S., Pusch, G.D., Shukla, M., Singh, I., Stewart, L., Tan, G., Thomas, C., VanOeffelen, M., Vonstein, V., Wallace, Z.S., Warren, A.S., Wattam, A.R., Xia, F., Yoo, H., Zhang, Y., Zmasek, C.M., Scheuermann, R.H., Stevens, R.L., Introducing the Bacterial and Viral Bioinformatics Resource Center (BV-BRC): a resource combining PATRIC, IRD and ViPR. Nucleic Acids Res. 51 (2023), D678–D689, 10.1093/nar/gkac1003.
Pallavi, B., Puneeth, T.G., Shekar, M., Girisha, S.K., Isolation, characterization and genomic analysis of vB-AhyM-AP1, a lytic bacteriophage infecting Aeromonas hydrophila. J. Appl. Microbiol. 131 (2021), 695–705, 10.1111/jam.14997.
Paquet, V.E., Vincent, A.T., Moineau, S., Charette, S.J., Beyond the A-layer: adsorption of lipopolysaccharides and characterization of bacteriophage-insensitive mutants of Aeromonas salmonicida subsp. salmonicida. Mol. Microbiol. 112 (2019), 667–677, 10.1111/mmi.14308.
Park, S.Y., Han, J.E., Kwon, H., Park, S.C., Kim, J.H., Recent insights into Aeromonas salmonicida and its bacteriophages in aquaculture: A comprehensive review. J. Microbiol. Biotechnol. 10 (2020), 1443–1457, 10.4014/JMB.2005.05040.
Pereira, C., Duarte, J., Costa, P., Braz, M., Almeida, A., Bacteriophages in the control of Aeromonas sp. in aquaculture systems: An integrative view. Antibiotics, 11, 2022, 163, 10.3390/ANTIBIOTICS11020163.
Richter, M., Rosselló-Móra, R., Oliver Glöckner, F., Peplies, J., JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32 (2016), 929–931, 10.1093/BIOINFORMATICS/BTV681.
Roberts, R.J., The Bacteriology of Teleosts. Roberts, R.J., (eds.) Fish Pathology, fourth ed, 2012, Wiley, 339–382, 10.1002/9781118222942.
Rostang, A., Bachelet, F., Fournel, C., Carabin, T., Navarro-Gonzalez, N., Calvez, S., Susceptibility of Aeromonas salmonicida subsp. salmonicida bacteria from French farmed trout to antibiotics commonly used in fish farming, and attempt to set epidemiological cut-off values. Front. Microbiol., 16, 2025, 1532748, 10.3389/FMICB.2025.1532748/BIBTEX.
Santos, L., Ramos, F., Antimicrobial resistance in aquaculture: Current knowledge and alternatives to tackle the problem. Int. J. Antimicrob. Agents 52 (2018), 135–143, 10.1016/J.IJANTIMICAG.2018.03.010.
Turner, D., Shkoporov, A.N., Lood, C., Millard, A.D., Dutilh, B.E., Alfenas-Zerbini, P., van Zyl, L.J., Aziz, R.K., Oksanen, H.M., Poranen, M.M., Kropinski, A.M., Barylski, J., Brister, J.R., Chanisvili, N., Edwards, R.A., Enault, F., Gillis, A., Knezevic, P., Krupovic, M., Kurtböke, I., Kushkina, A., Lavigne, R., Lehman, S., Lobocka, M., Moraru, C., Moreno Switt, A., Morozova, V., Nakavuma, J., Reyes Muñoz, A., Rūmnieks, J., Sarkar, B., Sullivan, M.B., Uchiyama, J., Wittmann, J., Yigang, T., Adriaenssens, E.M., Abolishment of morphology-based taxa and change to binomial species names: 2022 taxonomy update of the ICTV bacterial viruses subcommittee. Arch. Virol., 168, 2023, 74, 10.1007/S00705-022-05694-2.
Tynecki, P., Guziński, A., Kazimierczak, J., Jadczuk, M., Dastych, J., Onisko, A., PhageAI - Bacteriophage life cycle recognition with machine learning and natural language processing. bioRxiv, 2020, 2020.07.11.198606, 10.1101/2020.07.11.198606.
Van Twest, R., Kropinski, A.M., Bacteriophage enrichment from water and soil. Clokie, M.R.J., Kropinski, A.M., (eds.) Bacteriophages, first ed, 2009, Humana Press, New Jersey, 10.1007/978-1-60327-164-6.
Vincent, A.T., Paquet, V.E., Bernatchez, A., Tremblay, D.M., Moineau, S., Charette, S.J., Characterization and diversity of phages infecting Aeromonas salmonicida subsp. salmonicida. Sci. Rep., 7, 2017, 1054, 10.1038/S41598-017-07401-7.
Walker, B.J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S., Cuomo, C.A., Zeng, Q., Wortman, J., Young, S.K., Earl, A.M., Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One, 9, 2014, e112963, 10.1371/JOURNAL.PONE.0112963.