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Identification and Histopathology of Staphylococcus warneri in Rainbow Trout (Oncorhynchus mykiss)

Year 2023, Volume: 19 Issue: 3, 277 - 288, 01.09.2023
https://doi.org/10.22392/actaquatr.1276536

Abstract

This study was conducted to identify the disease that caused mortality in rainbow trout (Oncorhynchus mykiss) farms in the Aegean and Mediterranean regions in March 2022. External examination of infected trout revealed bilateral exophthalmos, hemorrhage in the lower jaw, dropsy, anemia in the liver, yellow exudate accumulation in the digestive system, hemorrhage in the adipose tissue and anus area, and spleen enlargement. A Gram-positive bacterium, Staphylococcus warneri, was isolated from infected fish's liver and anterior kidney. S. warneri was identified using morphological features, some conventional biochemical tests, and molecular genetic methods utilizing the 16S rRNA and sodA gene regions. Histopathological examination showed infiltration in the liver tissue, hyperemia in the spleen tissue, and necrotic changes in the kidney tubular epithelium of infected fish. According to the disk diffusion method, doxycycline was determined to be the most sensitive antibiotic against the S. warneri isolate. Although S. warneri was isolated in previous studies on rainbow trout, its histopathological effects on organs were determined for the first time in this study.

References

  • Akaylı, T., Ürkü, Ç., & Başaran, B. (2011). Kültür balıklarında Staphylococcus cohnii subsp. cohnii enfeksiyonu. Aquatic Sciences and Engineering, 26(2), 1-12.
  • Akayli, T., Urku, C., & Bozkurt, E. R. (2019). Determination of Co-infection in Diseased Seven khramulya (Capoeta capoeta). Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 22(6), 965-971. https://doi.org/10.18016/ksutarimdoga.vi.544200
  • Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389-3402. https://doi.org/10.1093/nar/25.17.3389
  • Atanasoff, A., & Urku, C. (2022). Isolation of Staphylococcus pasteuri in the cultured Russian sturgeon (Acipenser gueldenstaedtii) in Bulgarıa. JAPS: Journal of Animal & Plant Sciences, 32(4), 961-967. http://doi.org/10.36899/JAPS.2022.4.0498
  • Bancroft, J. D. & Stevens, A. (1990). Theory and practice of histopathological techniques (3rd ed.). Churchill Livingstone.
  • Bergey, D. H., & Holt, J. G. (1994). Bergey’s Manual of Determinative Bacteriology (9th Edition). Williams & Wilkins. Codoncode Aligner, CodonCode Corporation. Available from https://www.codoncode.com/index.htm (Erişim tarihi: 26.07.2022).
  • Çanak, Ö., & Timur, G. (2020). An initial survey on the occurrence of staphylococcal infections in Turkish marine aquaculture (2013–1014). Journal of Applied Ichthyology, 36(6), 932-941. https://doi.org/10.1111/jai.14141
  • Ghebremedhin, B., Layer, F., Konig, W., & Konig, B. (2008). Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. Journal of Clinical Microbiology 46(3), 1019–1025. https://doi.org/10.1128/JCM.02058-07
  • Gil, P., Vivas, J., Gallardo, C. S., & Rodriguez, L. A. (2000). First isolation of Staphylococcus warneri, from diseased rainbow trout, Oncorhynchus mykiss (Walbaum), in northwest Spain. Journal of Fish Diseases, 23(4), 295-298. http://dx.doi.org/10.1046/j.1365-2761.2000.00244.x
  • Haag, A. F., Fitzgerald, J. R., & Penadés, J. R. (2019). Staphylococcus aureus in Animals. Microbiology Spectrum, 7(3), 7-3. http://dx.doi.org/10.1128/microbiolspec.GPP3-0060-2019
  • Hoag A. F., Fitzgerald, J. R., & Penades, J. R. (2019). Staphylococcuc aureus in Animals. American Society For Microbiology. 7(3), 11. https://doi.org/10.1128/microbiolspec.GPP3-0060-2019
  • Huang, S. L., Chen, W. C., Shei, M. C., Liao, I. C., & Chen, S. N. (1999). Studies on epizootiology and pathogenecity of Staphylococcus epidermidis in tilapia (Oreochromis spp.) cultured in Taiwan. Zoological Studies, 38(2), 178-188.
  • Kim, J., Hong, J., Lim, J. A., Heu, S., & Roh, E. (2018). Improved multiplex PCR primers for rapid identification of coagulase-negative staphylococci. Archives of microbiology, 200(1), 73-83. https://doi.org/10.1007/s00203-017-1415-9
  • Korun, J., Yılmaz, M., Gökoğlu, M., & Çelik, Y. (2019). Isolation of Staphylococcus hominis from cultured gilthead sea bream (Sparus aurata L.) in Antalya Bay, Turkey. Journal of Agricultural Sciences, 25(1), 123-128. https://doi.org/10.15832/ankutbd.539018
  • Kubilay, A., & Ulukoy, G. (2004). First isolation of Staphylococcus epidermidis from cultured gilthead seabream (Sparus aurata) in Turkey. Bulletin of European Association of Fish Pathologists, 24(3), 137–143. https://hdl.handle.net/20.500.12809/5368
  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547-1549. https://doi.org/10.1093/molbev/msy096
  • Kusuda, R., & Sugıyama, A. (1981). Studies on the Characters of Staphylococcus epidermidis Isolated from Diseased Fishes-I On the Morphological, Biological and Biochemical Properties. Fish Pathology, 16(1), 15-24. https://doi.org/10.3147/jsfp.16.15
  • Marchesi, J. R., Sato, T., Weightman, A. J., Martin, T. A., Fry, J. C., Hiom, S. J., & Wade, W. G. (1998). Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Applied and environmental microbiology, 64(2), 795-799. https://doi.org/10.1128/AEM.64.2.795-799.1998
  • Metin, S., Kubilay, A., Onuk, E. E., Didinen, B. I., & Yildirim, P. (2014). First isolation of Staphylococcus warneri from cultured rainbow trout (Oncorhynchus mykiss) broodstock in Turkey. Bulletin of the European Association of Fish Pathologists, 34(5), 165-174.
  • Musharrafieh, R., Tacchi, L., Trujeque, J., LaPatra, S., & Salinas, I. (2014). Staphylococcus warneri, a resident skin commensal of rainbow trout (Oncorhynchus mykiss) with pathobiont characteristics. Veterinary microbiology, 169(1-2), 80-88. https://doi.org/10.1016/j.vetmic.2013.12.012
  • Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular biology and evolution. 25. 1253-6. https://doi.org/10.1093/molbev/msn083
  • Rambaut, A. (2014). Figtree v1.4.2. Available at http://tree.bio.ed.ac.uk/software/figtree (Erişim tarihi: 26.07.2022).
  • Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539-542. https://doi.org/10.1093/sysbio/sys029
  • Rusev, V., Rusenova, N., Simeonov, R., & Stratev, D. (2016). Staphylococcus warneri and Shewanella putrefaciens Co-infection in Siberian Sturgeon (Acipenser baerii) and Hybrid Sturgeon (Huso huso x Acipenser baerii). Journal of Microbiology & Experimentation, 3(1), 00078. http://dx.doi.org/10.15406/jmen.2016.03.00078
  • Shah, K. L., & Tyagi, B. C. (1986). An eye disease in silver carp, Hypophthalmichthys molitrix, held in tropical ponds, associated with the bacterium Staphylococcus aureus. Aquaculture, 55(1), 1-4. https://doi.org/10.1016/0044-8486(86)90050-5
  • Taponen, S., & Pyörälä, S. (2009). Coagulase-negative staphylococci as cause of bovine mastitis—Not so different from Staphylococcus aureus? Veterinary microbiology, 134(1-2), 29-36. https://doi.org/10.1016/j.vetmic.2008.09.011
  • Timur, G., & Akayli, T. (2003, 23-26 October). First study of staphylococcosis in farmed rain-bow trout (Oncorhynchus mykiss) fry in Turkey. International symposium on fisheries & zoology, Istanbul, Turkey.
  • Turgay, E., Karataş Stenium, S., & Candan, A. (2015). Kültürü yapılan gökkuşağı alabalıklarında (Oncorhynchus mykiss) Staphylococcus hominis subsp. hominis enfeksiyonu. Aquatic Sciences and Engineering, 30(1), 11-22. https://doi.org/10.18864/iujfas.86779
  • Wang, W. S., Chang, Y. C., Shieh, M. T., & Lin, C. C. (1996). Staphylococcus epidermidis and cestode infection of cultured grass carp (Ctenopharyngodon idella) in Taiwan. Reports on Fish Disease Research, 17, 57-63.
  • Weinstein, M. P., & Lewis, J. S. (2020). The clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: background, organization, functions, and processes. Journal of Clinical Microbiology, 58(3), e01864-19. https://doi.org/10.1128/JCM.01864-19
  • Wood, C. A. (1992). Significant infection caused by Staphylococcus warneri. Journal of Clinical Microbiology, 30(8), 2216. https://doi.org/10.1128%2Fjcm.30.8.2216-2217.1992
  • Xiao, Z., Xue, M., Wu, X., Zeng, L., Zhu, Y., Jiang, N., Fan, Y., & Zhou, Y. (2022). Isolation and identification of Staphylococcus warneri from diseased Coreius guichenoti. Aquaculture Reports, 22, 100988. https://doi.org/10.1016/j.aqrep.2021.100988

Gökkuşağı Alabalıklarında (Oncorhynchus mykiss) Staphylococcus warneri’ nin Teşhis ve Histopatolojisi

Year 2023, Volume: 19 Issue: 3, 277 - 288, 01.09.2023
https://doi.org/10.22392/actaquatr.1276536

Abstract

Bu çalışma, Ege ve Akdeniz bölgesinde bulunan gökkuşağı alabalığı (Oncorhynchus mykiss) çiftliklerinde Mart 2022 tarihinde mortaliteye neden olan hastalığın tanımlanması amacıyla yürütülmüştür. Enfekte alabalıkların dış incelemelerinde gözlerde bilateral ekzoftalmus, alt çenede kanama, dropsi, internal olarak karaciğerde anemi, sindirim sisteminde sarı eksüdat birikimi, yağ dokusunda ve anüs bölgesinde kanama, dalakta büyüme görüldü. Enfekte balıkların karaciğer ve ön böbreğinden Gram-pozitif bir bakteri olan Staphylococcus warneri izole edildi. S. warneri, morfolojik özellikleri, bazı geleneksel testler ve 16S rRNA ve sodA gen bölgeleri kullanılarak moleküler genetik yöntemler yardımıyla teşhis edildi. Histopatolojik incelemelerde enfekte balıkların karaciğer dokusunda infiltrasyon, dalak dokusunda hiperemi ve böbrek tübül epitelinde nekrotik değişiklikler saptandı. Disk difüzyon yöntemine göre S. warneri izolatının en duyarlı olduğu antibiyotiğin doxycycline olduğu belirlendi. Gökkuşağı alabalıklarında yapılan daha önceki çalışmalarda S. warneri türü izole edilmekle birlikte bu çalışma ile ilk kez S. warneri türünün organlardaki histopatolojik etkileri belirlenmiştir.

References

  • Akaylı, T., Ürkü, Ç., & Başaran, B. (2011). Kültür balıklarında Staphylococcus cohnii subsp. cohnii enfeksiyonu. Aquatic Sciences and Engineering, 26(2), 1-12.
  • Akayli, T., Urku, C., & Bozkurt, E. R. (2019). Determination of Co-infection in Diseased Seven khramulya (Capoeta capoeta). Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 22(6), 965-971. https://doi.org/10.18016/ksutarimdoga.vi.544200
  • Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389-3402. https://doi.org/10.1093/nar/25.17.3389
  • Atanasoff, A., & Urku, C. (2022). Isolation of Staphylococcus pasteuri in the cultured Russian sturgeon (Acipenser gueldenstaedtii) in Bulgarıa. JAPS: Journal of Animal & Plant Sciences, 32(4), 961-967. http://doi.org/10.36899/JAPS.2022.4.0498
  • Bancroft, J. D. & Stevens, A. (1990). Theory and practice of histopathological techniques (3rd ed.). Churchill Livingstone.
  • Bergey, D. H., & Holt, J. G. (1994). Bergey’s Manual of Determinative Bacteriology (9th Edition). Williams & Wilkins. Codoncode Aligner, CodonCode Corporation. Available from https://www.codoncode.com/index.htm (Erişim tarihi: 26.07.2022).
  • Çanak, Ö., & Timur, G. (2020). An initial survey on the occurrence of staphylococcal infections in Turkish marine aquaculture (2013–1014). Journal of Applied Ichthyology, 36(6), 932-941. https://doi.org/10.1111/jai.14141
  • Ghebremedhin, B., Layer, F., Konig, W., & Konig, B. (2008). Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. Journal of Clinical Microbiology 46(3), 1019–1025. https://doi.org/10.1128/JCM.02058-07
  • Gil, P., Vivas, J., Gallardo, C. S., & Rodriguez, L. A. (2000). First isolation of Staphylococcus warneri, from diseased rainbow trout, Oncorhynchus mykiss (Walbaum), in northwest Spain. Journal of Fish Diseases, 23(4), 295-298. http://dx.doi.org/10.1046/j.1365-2761.2000.00244.x
  • Haag, A. F., Fitzgerald, J. R., & Penadés, J. R. (2019). Staphylococcus aureus in Animals. Microbiology Spectrum, 7(3), 7-3. http://dx.doi.org/10.1128/microbiolspec.GPP3-0060-2019
  • Hoag A. F., Fitzgerald, J. R., & Penades, J. R. (2019). Staphylococcuc aureus in Animals. American Society For Microbiology. 7(3), 11. https://doi.org/10.1128/microbiolspec.GPP3-0060-2019
  • Huang, S. L., Chen, W. C., Shei, M. C., Liao, I. C., & Chen, S. N. (1999). Studies on epizootiology and pathogenecity of Staphylococcus epidermidis in tilapia (Oreochromis spp.) cultured in Taiwan. Zoological Studies, 38(2), 178-188.
  • Kim, J., Hong, J., Lim, J. A., Heu, S., & Roh, E. (2018). Improved multiplex PCR primers for rapid identification of coagulase-negative staphylococci. Archives of microbiology, 200(1), 73-83. https://doi.org/10.1007/s00203-017-1415-9
  • Korun, J., Yılmaz, M., Gökoğlu, M., & Çelik, Y. (2019). Isolation of Staphylococcus hominis from cultured gilthead sea bream (Sparus aurata L.) in Antalya Bay, Turkey. Journal of Agricultural Sciences, 25(1), 123-128. https://doi.org/10.15832/ankutbd.539018
  • Kubilay, A., & Ulukoy, G. (2004). First isolation of Staphylococcus epidermidis from cultured gilthead seabream (Sparus aurata) in Turkey. Bulletin of European Association of Fish Pathologists, 24(3), 137–143. https://hdl.handle.net/20.500.12809/5368
  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547-1549. https://doi.org/10.1093/molbev/msy096
  • Kusuda, R., & Sugıyama, A. (1981). Studies on the Characters of Staphylococcus epidermidis Isolated from Diseased Fishes-I On the Morphological, Biological and Biochemical Properties. Fish Pathology, 16(1), 15-24. https://doi.org/10.3147/jsfp.16.15
  • Marchesi, J. R., Sato, T., Weightman, A. J., Martin, T. A., Fry, J. C., Hiom, S. J., & Wade, W. G. (1998). Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Applied and environmental microbiology, 64(2), 795-799. https://doi.org/10.1128/AEM.64.2.795-799.1998
  • Metin, S., Kubilay, A., Onuk, E. E., Didinen, B. I., & Yildirim, P. (2014). First isolation of Staphylococcus warneri from cultured rainbow trout (Oncorhynchus mykiss) broodstock in Turkey. Bulletin of the European Association of Fish Pathologists, 34(5), 165-174.
  • Musharrafieh, R., Tacchi, L., Trujeque, J., LaPatra, S., & Salinas, I. (2014). Staphylococcus warneri, a resident skin commensal of rainbow trout (Oncorhynchus mykiss) with pathobiont characteristics. Veterinary microbiology, 169(1-2), 80-88. https://doi.org/10.1016/j.vetmic.2013.12.012
  • Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular biology and evolution. 25. 1253-6. https://doi.org/10.1093/molbev/msn083
  • Rambaut, A. (2014). Figtree v1.4.2. Available at http://tree.bio.ed.ac.uk/software/figtree (Erişim tarihi: 26.07.2022).
  • Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539-542. https://doi.org/10.1093/sysbio/sys029
  • Rusev, V., Rusenova, N., Simeonov, R., & Stratev, D. (2016). Staphylococcus warneri and Shewanella putrefaciens Co-infection in Siberian Sturgeon (Acipenser baerii) and Hybrid Sturgeon (Huso huso x Acipenser baerii). Journal of Microbiology & Experimentation, 3(1), 00078. http://dx.doi.org/10.15406/jmen.2016.03.00078
  • Shah, K. L., & Tyagi, B. C. (1986). An eye disease in silver carp, Hypophthalmichthys molitrix, held in tropical ponds, associated with the bacterium Staphylococcus aureus. Aquaculture, 55(1), 1-4. https://doi.org/10.1016/0044-8486(86)90050-5
  • Taponen, S., & Pyörälä, S. (2009). Coagulase-negative staphylococci as cause of bovine mastitis—Not so different from Staphylococcus aureus? Veterinary microbiology, 134(1-2), 29-36. https://doi.org/10.1016/j.vetmic.2008.09.011
  • Timur, G., & Akayli, T. (2003, 23-26 October). First study of staphylococcosis in farmed rain-bow trout (Oncorhynchus mykiss) fry in Turkey. International symposium on fisheries & zoology, Istanbul, Turkey.
  • Turgay, E., Karataş Stenium, S., & Candan, A. (2015). Kültürü yapılan gökkuşağı alabalıklarında (Oncorhynchus mykiss) Staphylococcus hominis subsp. hominis enfeksiyonu. Aquatic Sciences and Engineering, 30(1), 11-22. https://doi.org/10.18864/iujfas.86779
  • Wang, W. S., Chang, Y. C., Shieh, M. T., & Lin, C. C. (1996). Staphylococcus epidermidis and cestode infection of cultured grass carp (Ctenopharyngodon idella) in Taiwan. Reports on Fish Disease Research, 17, 57-63.
  • Weinstein, M. P., & Lewis, J. S. (2020). The clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: background, organization, functions, and processes. Journal of Clinical Microbiology, 58(3), e01864-19. https://doi.org/10.1128/JCM.01864-19
  • Wood, C. A. (1992). Significant infection caused by Staphylococcus warneri. Journal of Clinical Microbiology, 30(8), 2216. https://doi.org/10.1128%2Fjcm.30.8.2216-2217.1992
  • Xiao, Z., Xue, M., Wu, X., Zeng, L., Zhu, Y., Jiang, N., Fan, Y., & Zhou, Y. (2022). Isolation and identification of Staphylococcus warneri from diseased Coreius guichenoti. Aquaculture Reports, 22, 100988. https://doi.org/10.1016/j.aqrep.2021.100988
There are 32 citations in total.

Details

Primary Language Turkish
Subjects Structural Biology
Journal Section Research Articles
Authors

Öznur Diler 0000-0003-0330-3448

Hasan Emre Yılmaz 0000-0001-7953-3245

İfakat Tulay Çağatay 0000-0002-1868-8611

Mevlüt Nazıroğlu 0000-0003-0330-3448

Öznur Özil 0000-0003-2404-1328

Şeydanur Kan 0000-0002-0869-3628

Early Pub Date August 25, 2023
Publication Date September 1, 2023
Published in Issue Year 2023 Volume: 19 Issue: 3

Cite

APA Diler, Ö., Yılmaz, H. E., Çağatay, İ. T., Nazıroğlu, M., et al. (2023). Gökkuşağı Alabalıklarında (Oncorhynchus mykiss) Staphylococcus warneri’ nin Teşhis ve Histopatolojisi. Acta Aquatica Turcica, 19(3), 277-288. https://doi.org/10.22392/actaquatr.1276536