Pinpointing the role of Aeromonas salmonicida in the development of skin ulcerations in common dab (Limanda limanda).

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Source:
      Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 9881188 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2761 (Electronic) Linking ISSN: 01407775 NLM ISO Abbreviation: J Fish Dis Subsets: MEDLINE
    • Publication Information:
      Original Publication: Oxford, Blackwell Scientific Publications.
    • Subject Terms:
    • Abstract:
      Aeromonas salmonicida was isolated from ulcerations in common dab (Limanda limanda). An experiment was performed to pinpoint its role in ulceration development, considering the importance of the skin barrier and the pigmented and non-pigmented sides. The skin of dab was treated in three zones, one where scales and epidermis were removed, one where mucus was discarded and one non-treated zone. Fish were tagged to allow individual identification and challenged with A. salmonicida. Mortality and severity of the developing lesions were recorded for 21 days post-inoculation. Starting 12 days post-inoculation, mortality occurred gradually in challenged fish; however, no direct cause could be established. Both control fish and challenged fish developed ulcerations containing A. salmonicida. Sequencing of vapA gene revealed that isolates retrieved from both groups were distinct, suggesting the presence of A. salmonicida prior to the trial. Most ulcerations developed in zones where skin was removed, suggesting that abrasion might be a predisposing factor in ulceration development. Ulcerations were also observed at the insertion site of the tag, where exposed muscle tissue might have favoured the development of ulcerations. In conclusion, A. salmonicida seems to be involved in the development of skin ulcerations in dab, although the exact pathogenesis needs to be elucidated.
      (© 2020 John Wiley & Sons Ltd.)
    • References:
      Austin, B., & Austin, D. A. (2012). Bacterial fish pathogen: Disease of farmed and wild fish (6th ed.), The Netherlands:Springer. https://doi.org/10.1007/978-94-007-4884-2.
      Bartkova, S., Kokotovic, B., & Dalsgaard, I. (2017). Infection routes of Aeromonas salmonicida in rainbow trout monitored in vivo by real-time bioluminescence imaging. Journal of Fish Diseases, 40, 73-82. https://doi.org/10.1111/jfd.12491.
      Bouck, G. R., & Smith, S. D. (1979). Mortality of experimentally descaled smolts of coho salmon (Oncorhynchus kisutch) in fresh and salt water. Transactions of the American Fisheries Society, 108, 67-69. https://doi.org/10.1577/1548-8659(1979)108<67:MOEDSO>2.0.CO;2.
      Bruno, D. W. (2015). Furunculosis. Revised edition. ICES identification leaflets for diseases and parasites of fish and shellfish (p. 5). Leaflet No. 37. ICES.
      Burr, S. E., Pugovkin, D., Wahli, T., Segner, H., & Frey, J. (2005). Attenuated virulence of an Aeromonas salmonicida subsp. salmonicida type III secretion mutant in a rainbow trout model. Microbiology, 151, 2111-2118. https://doi.org/10.1099/mic.0.27926-0.
      Carlisle, J. C., & Roberts, R. J. (1977). An epidermal papilloma of the Atlantic salmon, I: Epizootiology, pathology and immunology. Journal of Wildlife Diseases, 13, 230-234. https://doi.org/10.7589/0090-3558-13.3.230.
      Dallaire-Dufresne, S., Tanaka, K. H., Trudel, M. V., Lafaille, A., & Charette, S. J. (2014). Virulence, genomic features, and plasticity of Aeromonas salmonicida subsp. salmonicida, the causative agent of fish furunculosis. Veterinary Microbiology, 169, 1-7. https://doi.org/10.1016/j.vetmic.2013.06.025.
      Davis, M. W., & Ottmar, M. L. (2006). Wounding and reflex impairment may be predictors for mortality in discarded or escaped fish. Fisheries Research, 82, 1-6. https://doi.org/10.1016/j.fishres.2006.09.004.
      Devriese, L., Soetaert, M., Bekaert, K., Desender, M., Chiers, K., & Decostere, A. (2015). Huidzweren bij vissen in het Belgische deel van de Noordzee: Trends in prevalentie en exploratie van mogelijke oorzaken (p. 188). Belgium: Research Institute for Agriculture, Fisheries and Food (ILVO), ILVO-Mededeling No. 188.
      Dodsworth, S. J., Bennett, A. J., & Coleman, G. (1993). Molecular cloning and nucleotide sequence analysis of the maltose-inducible porin gene of Aeromonas salmonicida. FEMS Microbiology Letters, 112, 191-198. https://doi.org/10.1111/j.1574-6968.1993.tb06447.x.
      Elliott, D. G., & Shotts, E. B. (1980). Aetiology of an ulcerative disease in goldfish Carassius auratus (L.): Microbiological examination of diseased fish from seven locations. Journal of Fish Diseases, 3, 133-143. https://doi.org/10.1111/j.1365-2761.1980.tb00196.x.
      Ellis, A. E., Hastings, T. S., & Munro, A. L. S. (1981). The role of Aeromonas salmonicida extracellular products in the pathology of furunculosis. Journal of Fish Diseases, 4, 41-51. https://doi.org/10.1111/j.1365-2761.1981.tb01108.x.
      Faílde, L. D., Bermúdez, R., Vigliano, F., Coscelli, G. A., & Quiroga, M. I. (2014). Morphological, immunohistochemical and ultrastructural characterization of the skin of turbot (Psetta maxima L.). Tissue and Cell, 46, 334-342. https://doi.org/10.1016/j.tice.2014.06.004.
      Fijan, N. N. (1972). Infectious dropsy in carp-a disease complex. Symposia of the Zoological Society of London, 30, 39-51.
      Fulton, T. W. (1904). The rate of growth of fishes. Twenty-second Annual Report, part III. (pp. 141-241). Edinburgh, Scotland: Fisheries Board of Scotland.
      Gavin, R., Rabaan, A. A., Merino, S., Tomas, J. M., Gryllos, I., & Shaw, J. G. (2002). Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Molecular Microbiology, 43, 383-397. https://doi.org/10.1046/j.1365-2958.2002.02750.x.
      Goodwin, A. E., & Merry, G. E. (2009). Are all koi ulcer cases associated with infection by atypical Aeromonas salmonicida? Polymerase chain reaction assays of koi carp skin swabs submitted by hobbyists. Journal of Aquatic Animal Health, 21, 98-103. https://doi.org/10.1577/H08-042.1.
      Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59, 307-321. https://doi.org/10.1093/sysbio/syq010.
      Gulla, S., Bayliss, S., Björnsdóttir, B., Dalsgaard, I., Haenen, O., Jansson, E., … Colquhoun, D. J. (2019). Biogeography of the fish pathogen Aeromonas salmonicida inferred by vapA genotyping. FEMS Microbiology Letters, 366, fnz074. https://doi.org/10.1093/femsle/fnz074.
      Gulla, S., Lund, V., Kristoffersen, A. B., Sørum, H., & Colquhoun, D. J. (2016). VapA (A-layer) typing differentiates Aeromonas salmonicida subspecies and identifies a number of previously undescribed subtypes. Journal of Fish Diseases, 39, 329-342. https://doi.org/10.1111/jfd.12367.
      Imsland, A. K., Olafsson, K., Skirnisdottir, S., Gunnarsson, S., Oddgeirsson, M., Vandamme, S., … Folkvord, A. (2014). Life history of turbot in Icelandic waters: Intra- and inter- population genetic diversity and otolith tracking of environmental temperatures. Fisheries Research, 155, 185-193. https://doi.org/10.1016/j.fishres.2014.03.004.
      Kirov, S. M., O’Donovan, L. A., & Sanderson, K. (1999). Functional characterization of type IV pili expressed on diarrhoea-associated isolates of Aeromonas species. Infection and Immunity, 67, 5447-5454.
      Lang, T., Mellegaard, S., Wosniok, W., Kadakas, V., & Neumann, K. (1999). Spatial distribution of grossly visible diseases and parasites in flounder (Platichthys flesus) from the Baltic Sea: A synoptic survey. ICES Journal of Marine Science, 56, 138-147. https://doi.org/10.1006/jmsc.1999.0465.
      Lang, T., Feist, S.W., Stentiford, G.D., Bignell, J.P., Vethaak, A.D., & Wosniok, W. (2017). Diseases of dab (Limanda limanda): Analysis and assessment of data on externally visible diseases, macroscopic liver neoplasms and liver histopathology in the North Sea, Baltic Sea and off Iceland. Marine Environmental Research, 124, 61-69.
      Larkin, Ma, Blackshields, G., Brown, Np, Chenna, R., McGettigan, Pa, McWilliam, H., Valentin, F., Wallace, Im, Wilm, A., Lopez, R., Thompson, Jd, Gibson, Tj, & Higgins, Dg (2007). Clustal W and clustal X version 2.0. Bioinformatics, 23, 2947-2948. https://doi.org/10.1093/bioinformatics/btm404.
      Law, M. (2001). Differential diagnosis of ulcerative lesions in fish. Environmental Health Perspectives, 109, 681-686. https://doi.org/10.2307/3454913.
      Mellergaard, S., & Nielsen, E. (1997). Epidemiology of lymphocystis, epidermal papilloma and skin ulcers in common dab Limanda limanda along the west coast of Denmark. Diseases of Aquatic Organisms, 30, 151-163. https://doi.org/10.3354/dao030151.
      Menanteau-Ledouble, S., Karsi, A., & Lawrence, M. L. (2011). Importance of skin abrasion as a primary site of adhesion for Edwardsiella ictaluri and impact on invasion and systematic infection in channel catfish Ictalurus punctatus. Veterinary Microbiology, 148, 425-430. https://doi.org/10.1016/j.vetmic.2010.08.022.
      Merino, S., Rubires, X., Aguilar, A., & Tomas, J. M. (1996). The O:34-antigen lipopolysaccharide as an adhesion in Aeromonas hydrophila. FEMS Microbiology Letters, 13, 97-101. https://doi.org/10.1111/j.1574-6968.1996.tb08186.x.
      Noga, E. J. (2000). Skin ulcers in fish: Pfiesteria and other etiologies. Toxicologic Pathology, 28, 807-823. https://doi.org/10.1177/019262330002800607.
      Pedersen, K., Kofod, H., Dalsgaard, I., & Larsen, J. L. (1994). Isolation of oxidase-negative Aeromonas salmonicida from diseased turbot Scophthalmus maximus. Diseases of Aquatic Organisms, 18, 149-154. https://doi.org/10.3354/dao018149.
      Reith, M. E., Singh, R. K., Curtis, B., Boyd, J. M., Bouevitch, A., Kimball, J., … Brown, L. L. (2008). The genome of Aeromonas salmonicida subsp. salmonicida A449: Insights into the evolution of a fish pathogen. BMC Genomics, 9, 427. https://doi.org/10.1186/1471-2164-9-427.
      Spinner, M., Kortmann, M., Traini, C., & Gorb, S. N. (2016). Key role of scale morphology in flatfishes (Pleuronectiformes) in the ability to keep sand. Scientific Reports, 6, https://doi.org/10.1038/srep26308.
      Svendsen, Y. S., & Bøgwald, J.. (1997). Influence of artificial wound and non-intact mucus layer on mortality of Atlantic salmon (Salmo salar L.) following a bath challenge with Vibrio anguillarum and Aeromonas salmonicida. Fish and Shellfish Immunology, 7, 317-325. https://doi.org/10.1006/fsim.1997.0087.
      Toranzo, A. E., & Barja, J. L. (1992). First report of furunculosis in turbot reared in floating cages in northwest of Spain. Bulletin of the European Association of Fish Pathologists, 12, 147-149.
      Vercauteren, M., De Swaef, E., Declercq, A. M., Bosseler, L., Gulla, S., Balboa, S., … Decostere, A. (2018). First isolation of Vibrio tapetis and an atypical strain of Aeromonas salmonicida from skin ulcerations in common dab (Limanda limanda) in the North Sea. Journal of Fish Diseases, 41, 329-335. https://doi.org/10.1111/jfd.12729.
      Vercauteren, M., De Swaef, E., Declercq, A. M., Polet, H., Aerts, J., Ampe, B., … Chiers, K. (2019). Scrutinizing the triad of Vibrio tapetis, the skin barrier and pigmentation as determining factors in the development of skin ulcerations in wild common dab (Limanda limanda). Veterinary Research, 50, 41. https://doi.org/10.1186/s13567-019-0659-6.
      Vethaak, A. D. (1992). Diseases of flounder (Platichthys Flesus L.) in the Dutch Wadden Sea, and their relation to stress factors. Netherlands Journal of Sea Research, 29, 257-272. https://doi.org/10.1016/0077-7579(92)90025-A.
      Virsek, M. K., Lovsin, M. N., Koren, S., Krzan, A., & Peterlin, M. (2017). Microplastics as a vector for the transport of the bacterial fish pathogen species Aeromonas salmonicida. Marine Pollution Bulletin, 125, 301-309. https://doi.org/10.1016/j.marpolbul.2017.08.024.
      Whitby, P. W., Landon, M., & Coleman, G. (1992). The cloning and nucleotide sequence of the serine protease gene (aspA) of Aeromonas salmonicida ssp. salmonicida. FEMS Microbiology Letters, 99, 65-72. https://doi.org/10.1111/j.1574-6968.1992.tb05543.x.
      Wiklund, T. (1990). Atypical Aeromonas salmonicida isolated from ulcers of pike Esox lucius L. Journal of Fish Diseases, 13, 541-544. https://doi.org/10.1111/j.1365-2761.1990.tb00815.x.
      Wiklund, T. (1994). Skin ulcer disease of flounder (Platichthys flesus): A review. In G. Bylund, & L. Lönn-ström (Eds.), Diseases and parasites of flounder (Platichthys flesus) in the northern Baltic sea (pp. 17-26). Finland:The Baltic Marine Biologists. https://doi.org/10.3354/dao017165.
      Wiklund, T. (1995). Virulence of ‘atypical’ Aeromonas salmonicida isolated from ulcerated flounder Platichthys flesus. Diseases of Aquatic Organisms, 21, 145-150. https://doi.org/10.3354/dao021145.
      Wiklund, T., & Bylund, G. (1993). Skin ulcer disease of flounder Platichthys flesus in the Northern Baltic Sea. Diseases of Aquatic Organisms, 17, 165-174. https://doi.org/10.3354/dao017165.
      Wiklund, T., & Dalsgaard, I. (1998). Occurrence and significance of atypical Aeromonas salmonicida in non-salmonid and salmonid fish species: A review. Diseases of Aquatic Organisms, 32, 49-69. https://doi.org/10.3354/dao032049.
      Wiklund, T., Tabolina, I., & Bezgachina, T. V. (1999). Recovery of atypical Aeromonas salmonicida from ulcerated fish from the Baltic Sea. ICES Journal of Marine Science, 56, 175-179. https://doi.org/10.1006/jmsc.1999.0464.
    • Grant Information:
      Vlaamse regering; EMBRC-ERIC; VIS/15/A03/DIV EUROPEAN Fisheries Fund; Research Foundation - Flanders (FWO)
    • Contributed Indexing:
      Keywords: Aeromonas salmonicida; A-layer typing; common dab; skin barrier; skin ulceration
    • Molecular Sequence:
      GENBANK MK244113; MK244206; NVI-09978; MK243982
    • Publication Date:
      Date Created: 20200110 Date Completed: 20200812 Latest Revision: 20200930
    • Publication Date:
      20240829
    • Accession Number:
      10.1111/jfd.13133
    • Accession Number:
      31918449