Research Article
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A mixed Bacillus gibsonii and Sphingomonas echinoides infection in cultured rainbow trout (Oncorhynchus mykiss)

Year 2021, Volume: 3 Issue: 2, 71 - 79, 31.12.2021
https://doi.org/10.51756/marlife.999539

Abstract

Rainbow trout (Oncorhynchus mykiss) is a fish species with a long history of cultivation and bacterial pathogens are limiting the success rate. The aim of this study is the biochemical and molecular identification of two opportunistic pathogens detected in the rainbow trout cultured in net cages in a dam lake located on the Kızılırmak river; revealing the pathological symptoms of them in the moribund fish samples; determination of their antimicrobial susceptibility profile and determination of the antagonistic effect of two probiotic-candidate strains against them. Depending on the results of the conventional bacteriologic and molecular identification studies, bacterial isolates recovered from the internal organs of the moribund fish samples, a mixed bacterial infection case of Bacillus gibsonii and Sphingomonas echinoides was identified in the moribund fish samples showing general bacterial hemorrhagic septicemia symptoms for the first time in rainbow trout. Despite it was not possible to identify these isolates at the species level using conventional bacteriological methods, our isolates separately showed similarities more than 99% with the above mentioned species in the 16s RNA sequence analysis. The results of this study showed that, long term water quality parameter determination and bacterial distribution monitoring studies which include molecular tools should be carried out in the aquaculture sites to increase the success in trout culture.

Supporting Institution

İstanbul Üniversitesi Bilimsel Araştırma Projeleri Birimi

Project Number

FBA-28476

Thanks

This study was supported by Istanbul University Research Projects coordination unit with the project number: FBA-2018-28476. The authors would like to thank other staff of the project, Dr. Eda YARDIMCI and Dilek OKMEN who were not added to the author list of this manuscript with their own request.The authors also would like to thank the staff of the fish farms for their valuable helps during field sampling.

References

  • Akaylı, T., Albayrak, G., Ürkü, Ç., Çanak, Ö. & Yörük, E. (2015). Characterization of Micrococcus luteus and Bacillus marisflavi recovered from Common Dentex (Dentex dentex) larviculture system. Mediterranean Marine Science, 17(1): 163-169.
  • Akaylı, T., Çanak, Ö., Yardımcı, R. E., Ürkü, Ç. & Ökmen, D. (2020). A mixed Frigoribacterium faeni and Lactococcus garvieae Infection in cultured Rainbow Trout (O. mykiss). KSU Journal of Agriculture and Nature, 23(6):1569-1577. https://doi.org/10.18016/ksutarimdoga.vi.707820
  • Akaylı, T., Çanak, Ö., Yardımcı, R. E., Ürkü, Ç. & Ökmen, D. (2021). Enterobacter infections of cultured Rainbow Trout (Oncorhynchus mykiss). Fresenius Environmental Bulletin, 30(11): 11942-11947.
  • Alipiah, N. M., Ramli, N. H. S., Low, C.F., Shamsudin, M. & Yusoff, F. M. (2016). Protective effects of Sea Cucumber surface-associated bacteria against Vibrio harveyi in Brown-Marbled Grouper fingerlings. Aquaculture Environment Interactions, 8:147-155.
  • Ashraf, A. (2000). Probiotics in fish farming-evaluation of a candidate bacterial mixture, Licentiate thesis, University of Umea.
  • Austin, B. & Austin, D. A. (2016). Bacterial fish pathogens, diseases of farmed and wild fish 6th edition. Springer, Dordrecht.
  • Ayaz, S. Ç., Aktaş, Ö., Dağlı, S., Aydöner, C., Atasoy Aytış, E. & Akça, L. (2012). Pollution loads and surface water quality in the Kızılırmak Basin, Turkey. Desalination and Water Treatment, 51(7-9):1533-1542. https://doi.org/10.1080/19443994.2012.698814
  • Bakan, G., Böke Özkoç, H., Tülek, S. & Cüce, H. (2010). Integrated environmental quality assessment of Kızılırmak River and its coastal environment. Turkish Journal of Fisheries and Aquatic Sciences, 10: 453-462. https://doi.org/10.4194/trjfas.2010.0403
  • Balkwill, D. L., Fredrickson, J. K. & Romine, M.F. (2006). Sphingomonas and related genera In: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., Stackebrandt, E. (Eds). TheProkaryotes. Springer-Verlag, New York.
  • Balta F. & Balta Z. D. (2019). The Isolation of Lactococcus garvieae from eyes of diseased Rainbow Trout (Oncorhynchus mykiss) with Exopthalmia. Journal of Anatolian Environmental and Animal Sciences, 4(1):27-33.
  • Batool, R., Rehman, S.U., Rafique, M., Amna, A. J., Mukhtar, T., Mahmood, S., Sultan, T., Munis, F.H. & Chaudhary, H.J. (2019). Biocontrol potential of Bacillus gibsonii and Brevibacterium frigoritolerans in suppression of fusarium stalk rot of maize: a sustainable approach. Asian Journal of Agriculture and Biology, 7(3):320-333.
  • Berrada, I., Benkhemmar, O., Swings, J., Bendaou, N. & Amar, M. (2012). Selection of Halophilic bacteria for biological control of Tomato gray mould caused by Botrytis cinerea. Phytopathologia Mediterranea, 51(3): 625-630.
  • Bhunia, A.K., Johnson, M.C. & Ray, B. (1988). Purification, characterization and antimicrobial spectrum of Bacteriocin produced by Pediococcus acidilactici. Jorunal of Applied Microbiology, 65: 261-268.
  • Brink, M., Rhode, C., Macey, B. M., Christison, K. W. & Rodot-Wilding, R. (2019). Metagenomic assessment of body surface bacterial communities of the Sea Urchin, Tripneustes gratilla. Marine Genomics, 47: 100675.
  • Burr, G., Gathlin, D. (2005). Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture. Journal of the World Aquaculture Society, 36: 425-436.
  • Cazorla, F. M., Romero, D., Perez-Garcia, A., Lugtenberg, L. J. J., de Vicente, A. & Bloemberg, G. (2007). Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. Journal of Applied Microbiology, 103: 1950-1959.
  • Das, B. K., Neha Nidhi, R. G., Roy, P., Muduli, A. K., Swain, P., Mishra, S. S. & Jayasankar, P. J. (2014). Antagonistic activity of cellular components of Bacillus subtilis AN11 against bacterial pathogens. International Journal of Current Microbiology & Applied Sciences, 3(5): 795-809.
  • Demirci, A. (2017). Isolation and characterization of various bacteria in some regional yoghurt samples in Ağrı. MSc. Thesis. Ağrı İbrahim Çeçen University, Institute of Science.
  • Deng, A., Zhang, G., Shi, N., Wu, J., Lu, F. & Wen, T. (2014). Secretory expression, functional characterization, and molecular genetic analysis of novel halo-solvent-tolerant protease from Bacillus gibsonii. Journal of Microbiology and Biotechnology, 24(2): 197-208.
  • Denner, E. B. M., Kämpfer, P., Busse, H. J. & Moore, E. R. B. (1999). Reclassification of Pseudomonas echinoides Heumann 1962, 343AL, in the genus Sphingomonas as Sphingomonas echinoides comb. nov. International Journal of Systematic Bacteriology, 49: 1103-1109.
  • Dönmez, Y. (2014). Studies on vegetation geography of Turkey. İstanbul Üniversitesi Edebiyat Fakültesi Coğrafya Bölümü Coğrafya Dergisi, 29: 1-27.
  • Engin, M. S., Uyanık, A. & Cay, S. (2017). Investigation of trace metals distribution in water, sediments and wetland plants of Kızılırmak Delta, Turkey. International Journal of Sediment Research, 32: 90-97.
  • Eski, A., Demir, İ., Sezen, K. & Demirbağ, Z. (2017). A new biopesticide from a local Bacillus thuringiensis var. tenebrionis (Xd3) against alder leaf beetle (Coleoptera: Chrysomelidae). World Journal of Microbiology and Biotechnology, 33(5): 95. https://doi.org/10.1007/s11274-017-2263-0
  • Fayol-Messaoudi, D., Coconnier-Polter, M. H., Lievin-Le Moal, V., Atassi, F., Berger, C. N. & Servin, A. L. (2007). The Lactobacillus plantarum Strain ACA-DC287 isolated from a Greek cheese demonstrates antagonistic activity in vitro and in vivo against Salmonella enterica serovar typhimurium. Journal of Applied Microbiology, 103: 657-665.
  • Fedorova, T. V., Vasina, D. V., Begunova, A. V., Rozhkova, I. V., Raskoshnaya, T. A. & Gabrielyan, N. I. (2018). Antagonistic activity of lactic acid bacteria Lactobacillus spp. against clinical isolates of Klebsiella pneumonia. Applied Biochemistry & Microbiology, 54(3): 277-287.
  • Garbeva, P., van Veen, J. A. & van Elsas, J. D. (2003). Predominant Bacillus spp. in agricultural soil under different management regimes detected via PCR-DGGE. Microbial Ecology, 45: 302-316. https://doi.org/10.1007/s00248-002-2034-8
  • Gomez-Gil, B., Roque, A. & Turnbull, J. F. (2000). The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms. Aquaculture, 191: 259-270.
  • Gopal, P. K., Prasad, J., Smart, J. & Gill, H. S. (2001). In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. International Journal of Food Microbiology, 67: 207-216.
  • Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 95-98.
  • Heumann, W. (1960). Versuche zur Rekombination Sternbildender Bakterien. Naturwissenschaften, 47: 330-331.
  • İçgen, B. & Yılmaz, F. (2014). Co-occurrence of antibiotic and heavy metal resistance in Kızılırmak River isolates. Bulletin of Environmental Contamination and Toxicology, 93: 735-743.
  • Irkitova, A. N., Grebenshchikova, A. V. & Matsyura, A. V. (2018). Antagonistic activity of Bacillus subtilis strains isolated from various sources. Ukrainian Journal of Ecology, 8(2): 354-364.
  • Jeong, S. J., Heo, K., Park, J. Y., Lee, K. W., Park, J. Y., Joo, S. H. & Kim, J. H. (2015). Characterization of AprE176, a fibrinolytic enzyme from Bacillus subtilis HK176. Journal of Microbiology and Biotechnology, 25(1): 89-97.
  • Kan, N. İ. & Sarıeyyüpoğlu, M. (2008). Investigation of streptococci in fish caught from region of Elaziğ city sewage discharged into Keban Dam Lake. Fırat Üniversitesi Fen Bilimleri Dergisi, 20(2): 271-277. (In Turkish)
  • Katırcıoğlu, H. (2001). Gökkuşağı Alabalığı ve Aynalı Sazandan izole edilen laktik asit bakterilerinin metabolik ve antimikrobiyal aktivitelerinin incelenmesi. Gazi Üniversitesi Fen Bilimleri Enstitüsü Biyoloji Ana Bilim Dalı, Doktora tezi, 139, Ankara.
  • Kavuthodi, B. & Sebastian, D. (2018). Review on bacterial production of alkaline pectinase with special emphasis on Bacillus species. Bioscience Biotechnology Research Communications, 11(1): 18-30.
  • Kim, H.S., Lee, O. K., Lee, S. J., Hwang, S., Kim, S. J., Yang, S. H., Park, S. & Lee, E. Y. (2006). Enantioselective epoxide hydrolase activity of a newly isolated microorganism, Sphingomonas echinoides EH-983, from seawater. Journal of Molecular Catalysis B: Enzymatic, 41: 130-135. https://doi.org/10.1016/j.molcatb.2006.05.009
  • Kimura, S., Bryan, C. G., Hallberg, K. B. & Johnson, D. B. (2011). Biodiversity and geochemistry of an extremely Acidic, low-temperature subterranean environment sustained by chemolithotrophy. Environmental Microbiology, 13(8):2092–2104. https://doi.org/10.1111/j.1462-2920.2011.02434.x
  • Lane, D.J. (1991). 16S/23S rRNA sequencing. In: Nucleic Acid Techniques in Bacterial Systematics, Ed. E. Stackebrandt and M. Goodfellow. John Wiley and Sons, Chichester. 115-175.
  • Larkin, M. A., Blackshields, G., Brown, N., Chenna, R., Mcgettigan, P. A., Mcwilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & Lopez, R. (2007). Clustal W and Clustal X version 2.0. Bioinformatics. 23: 2947-2948.
  • Lee, M. J., Lee, J. J., Chung, H. Y., Choi, S. H. & Kim, B. S. (2016). Analysis of microbiota on abalone (Haliotis discus hannai) in South Korea for Improved product management. International Journal of Food Microbiology, 234: 45-52.
  • Li, Z., Bai, Z., Zhang, B., Xie, H., Hu, Q., Hao, C., Xue, W. & Zhang, H. (2005). Newly isolated Bacillus gibsonii S-2 Capable of using sugar beet pulp for alkaline pectinase production. World Journal of Microbiology & Biotechnology, 21: 1483-1486. https://doi.org/10.1007/s11274-005-7025-8
  • Logan, N. A. & De Vos, P. (2009). Genus: Bacillus, Bergey’s manual of systematics bacteriology Vol III, Springer Dordrecht Heidelberg London New York, 21-128.
  • Ma, Y. X., Li, L. Y., Bao, P. Y., Li, M., Chen, W. & Chang Y. Q. (2018). Effects of combined dietary administration of Rhodotorula sp. H26 and Bacillus sp. BC26 on growth, immunity and intestinal microbiota in juvenile Sea Cucumber, Apostichopus japonicus. Aquaculture Research, 49: 3792-3803.
  • Muz, A., Sarıeyyüpoğlu, M., Ertaş, H. B. & Şimşek, A. (1995). Keban Baraj Gölü’nden yakalanan bazı balıkların aerobik ve mikroaerofilik bakteriler yönünden incelenmesi. Fırat Üniversitesi Sağlık Bilimleri Dergisi, 9(2): 212-219.
  • Nannan, C., Vu, H. Q., Gillis, A., Gaulier, S., Nguyen, T. T. T. & Mahillon, J. (2021). Bacilysin within the Bacillus subtilis Group: Gene Prevalence versus antagonistic activity against Gram-negative foodborne pathogens. Journal of Biotechnology, 327: 28-35.
  • Orozova, P., Sirakov, I., Austin, D. A. & Austin, B. (2018). Recovery of Bacillus mycoides, B. pseudomycoides and Aeromonas hydrophila from common carp (Cyprinus carpio) and Rainbow Trout (Oncorhynchus mykiss) with gill disease. Journal of Fish Diseases, 41(1): 125-129.
  • Özer, G., Ergene, A. & İçgen, B. (2013). Biochemical and molecular characterization of strontium-resistant environmental isolates of Pseudomonas fluorescens and Sphingomonas paucimobilis. Geomicrobiology Journal, 30: 381-390. https://doi.org/10.1080/01490451.2012.694977
  • Özer, S., Demirel, M., Us, M. & Yıldırım, S. (2008). Microbial flora of rainbow trout (Oncorhynchus mykiss, Walbaum) hatcheries in Çağlarca, province Mersin-Turkey. Journal of FisheriesSciences.com, 2(3): 261-271. (In Turkish) https://doi.org/10.3153/jfscom.mug.200713
  • Öztürk, T., Didinen, B. I., Doğan, G., Özer, A. & Bircan, R. (2013). Lactococcosis in Rainbow Trout (Oncorhynchus mykiss, Walbaum, 1792) in the Middle Black Sea Region in Turkey and antimicrobial susceptibility of the aetiological agent, Lactococcus garvieae. Etlik Vet Mikrobiyol Derg, 24:7-12.
  • Pandey, A. K., Patel, A. K., Banjare, U. & Singh, R. K. (2021). Molecular characterization of bacterial microbiome isolated from wheat rhizosphere of agro climatic zones of India. Indian Journal of Natural Sciences, 12(67): 33033-33042.
  • Piccini, C., Conde, D., Alonso, C., Sommaruga, R. & Pernthalter, J. (2006). Blooms of single bacterial species in a coastal lagoon of the Southwestern Atlantic Ocean. Applied and Environmental Microbiology, 72(10): 6560–6568. https://doi.org/10.1128/AEM.01089-06
  • Rafat, A., Philip, K. & Muniandy, S. (2012). A novel source of bioactive compounds: Endophytic bacteria isolated from Centella asiatica. Journal of Pure and Applied Microbiology, 6(1): 11-20.
  • Ringo, E. & Gatesoupe, F. J. (1998). Lactic acid bacteria in fish: a review. Aquaculture, 160: 177-203.
  • Roberts, R. J. (2012). Fish pathology 4th edition, Wiley-Blackwell, UK.
  • Sezen, K., İşci, Ş., Muratoğlu, H., İnan, K. & Demirbağ, Z. (2013). Identification and pathogenicity of bacteria from Gryllotalpa gryllotalpa L. (Orthoptera: Gryllotalpidae). Türkiye Biyolojik Mücadele Dergisi, 4(2): 89-108.
  • Shin, S. C., Kim, S. J., Ahn, D. H., Lee, J. K. & Park, H. (2012). Draft genome sequence of Sphingomonas echinoides ATCC 14820. Journal of Bacteriology, 194(7): 1843.
  • Singh, B. R., Agrawal, R., Vadhana, P., Bhardwaj, M. & Dubey, S. (2015). Antimicrobial activity of citronella essential oil on antimicrobial drug resistant bacteria from veterinary clinical cases. Clinical & Medical Biochemistry, 1(1): 1000106.
  • Tambekar, D. H. & Dhundale, V. R. (2012). Studies on the physiological and cultural diversity of bacilli characterized from Lonar Lake (Ms) India. Bioscience Discovery, 3(1): 34-39.
  • Taş, B. (2006). Investigation of water quality of Derbent Dam Lake (Samsun). Ekoloji, 60:1-6.
  • TUIK (2020). Turkish Statistical Institute Retrieved on November 06, 2020 from https://tuikweb.tuik.gov.tr/PreTablo.do?alt_id=1005
  • Tuo, Y., Zhang, W., Zhang, L., Ai, L., Zhang, Y., Han, X. & Yi, H. (2013). Study of probiotic potential of four wild Lactobacillus rhamnosus strains. Anaerobe, 21: 22-27.
  • Türe, M., Altınok, İ., Işıdan, H., Savaş, H. & Kutlu, İ. (2012). PFGE metodu kullanılarak Lactoccoccus garvieae’nin genetik çeşitliliğinin ve yayılımının belirlenmesi, TAGEM Proje Sonuç Raporu. Su Ürünleri Merkez Araştırma Enstitüsü, Trabzon.
  • Verdenelli, M. C., Ghelfi, F., Silvi, S., Orpianesi, C., Cecchini, C. & Cresci, A. (2009). Probiotic properties of Lactobacillus rhamnosus and Lactobacillus paracasei isolated from human faeces. European Journal of Nutrition, 48: 355-363.
  • Wikler, M. (2006). Performance Standards for Antimicrobial Susceptibility Testing. Wayne, PA; Clinical and Laboratory Standards Insitute.
  • Yabuuchi, E. & Kosako, Y. (2005). Genus: Sphingomonas Bergey’s manual of systematics bacteriology Vol II part C, Springer Dordrecht Heidelberg London New York, 21-128.
  • Yuan, X., Zhou, Y., Liang, X.F., Guo, X., Fang, L., Li, J., Liu, L. & Li, B. (2015). Effect of dietary glutathione supplementation on the biological value of rapeseed meal to juvenile Grass Carp, Ctenopharyngodon idellus. Aquaculture Nutrition, 21: 73-84. https://doi.org/10.1111/anu.12142
  • Zhang, B., Fan, R., Bai, Z., Wang, S., Wang, L. & Shi, J. (2013). Biosorption characteristics of Bacillus gibsonii S-2 waste biomass for removal of lead (II) from aqueous solution. Environmental Science and Pollution Research, 20: 1367-1373. https://doi.org/10.1007/s11356-012-1146-z
  • Zhang, Z., Schwartz, S., Wagner, L. & Miller, W. (2000). A greedy algorithm for aligning DNA sequences. Journal of Computational Biology, 7: 203-214.
  • Zhou, Y., Yuan, X., Liang, X.F., Fang, L., Li, J., Guo, X., Bai, X. & He, S. (2013). Enhancement of growth and intestinal flora in Grass Carp: The Effect of exogenous cellulose. Aquaculture, 416-417: 1-7.
Year 2021, Volume: 3 Issue: 2, 71 - 79, 31.12.2021
https://doi.org/10.51756/marlife.999539

Abstract

Project Number

FBA-28476

References

  • Akaylı, T., Albayrak, G., Ürkü, Ç., Çanak, Ö. & Yörük, E. (2015). Characterization of Micrococcus luteus and Bacillus marisflavi recovered from Common Dentex (Dentex dentex) larviculture system. Mediterranean Marine Science, 17(1): 163-169.
  • Akaylı, T., Çanak, Ö., Yardımcı, R. E., Ürkü, Ç. & Ökmen, D. (2020). A mixed Frigoribacterium faeni and Lactococcus garvieae Infection in cultured Rainbow Trout (O. mykiss). KSU Journal of Agriculture and Nature, 23(6):1569-1577. https://doi.org/10.18016/ksutarimdoga.vi.707820
  • Akaylı, T., Çanak, Ö., Yardımcı, R. E., Ürkü, Ç. & Ökmen, D. (2021). Enterobacter infections of cultured Rainbow Trout (Oncorhynchus mykiss). Fresenius Environmental Bulletin, 30(11): 11942-11947.
  • Alipiah, N. M., Ramli, N. H. S., Low, C.F., Shamsudin, M. & Yusoff, F. M. (2016). Protective effects of Sea Cucumber surface-associated bacteria against Vibrio harveyi in Brown-Marbled Grouper fingerlings. Aquaculture Environment Interactions, 8:147-155.
  • Ashraf, A. (2000). Probiotics in fish farming-evaluation of a candidate bacterial mixture, Licentiate thesis, University of Umea.
  • Austin, B. & Austin, D. A. (2016). Bacterial fish pathogens, diseases of farmed and wild fish 6th edition. Springer, Dordrecht.
  • Ayaz, S. Ç., Aktaş, Ö., Dağlı, S., Aydöner, C., Atasoy Aytış, E. & Akça, L. (2012). Pollution loads and surface water quality in the Kızılırmak Basin, Turkey. Desalination and Water Treatment, 51(7-9):1533-1542. https://doi.org/10.1080/19443994.2012.698814
  • Bakan, G., Böke Özkoç, H., Tülek, S. & Cüce, H. (2010). Integrated environmental quality assessment of Kızılırmak River and its coastal environment. Turkish Journal of Fisheries and Aquatic Sciences, 10: 453-462. https://doi.org/10.4194/trjfas.2010.0403
  • Balkwill, D. L., Fredrickson, J. K. & Romine, M.F. (2006). Sphingomonas and related genera In: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., Stackebrandt, E. (Eds). TheProkaryotes. Springer-Verlag, New York.
  • Balta F. & Balta Z. D. (2019). The Isolation of Lactococcus garvieae from eyes of diseased Rainbow Trout (Oncorhynchus mykiss) with Exopthalmia. Journal of Anatolian Environmental and Animal Sciences, 4(1):27-33.
  • Batool, R., Rehman, S.U., Rafique, M., Amna, A. J., Mukhtar, T., Mahmood, S., Sultan, T., Munis, F.H. & Chaudhary, H.J. (2019). Biocontrol potential of Bacillus gibsonii and Brevibacterium frigoritolerans in suppression of fusarium stalk rot of maize: a sustainable approach. Asian Journal of Agriculture and Biology, 7(3):320-333.
  • Berrada, I., Benkhemmar, O., Swings, J., Bendaou, N. & Amar, M. (2012). Selection of Halophilic bacteria for biological control of Tomato gray mould caused by Botrytis cinerea. Phytopathologia Mediterranea, 51(3): 625-630.
  • Bhunia, A.K., Johnson, M.C. & Ray, B. (1988). Purification, characterization and antimicrobial spectrum of Bacteriocin produced by Pediococcus acidilactici. Jorunal of Applied Microbiology, 65: 261-268.
  • Brink, M., Rhode, C., Macey, B. M., Christison, K. W. & Rodot-Wilding, R. (2019). Metagenomic assessment of body surface bacterial communities of the Sea Urchin, Tripneustes gratilla. Marine Genomics, 47: 100675.
  • Burr, G., Gathlin, D. (2005). Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture. Journal of the World Aquaculture Society, 36: 425-436.
  • Cazorla, F. M., Romero, D., Perez-Garcia, A., Lugtenberg, L. J. J., de Vicente, A. & Bloemberg, G. (2007). Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. Journal of Applied Microbiology, 103: 1950-1959.
  • Das, B. K., Neha Nidhi, R. G., Roy, P., Muduli, A. K., Swain, P., Mishra, S. S. & Jayasankar, P. J. (2014). Antagonistic activity of cellular components of Bacillus subtilis AN11 against bacterial pathogens. International Journal of Current Microbiology & Applied Sciences, 3(5): 795-809.
  • Demirci, A. (2017). Isolation and characterization of various bacteria in some regional yoghurt samples in Ağrı. MSc. Thesis. Ağrı İbrahim Çeçen University, Institute of Science.
  • Deng, A., Zhang, G., Shi, N., Wu, J., Lu, F. & Wen, T. (2014). Secretory expression, functional characterization, and molecular genetic analysis of novel halo-solvent-tolerant protease from Bacillus gibsonii. Journal of Microbiology and Biotechnology, 24(2): 197-208.
  • Denner, E. B. M., Kämpfer, P., Busse, H. J. & Moore, E. R. B. (1999). Reclassification of Pseudomonas echinoides Heumann 1962, 343AL, in the genus Sphingomonas as Sphingomonas echinoides comb. nov. International Journal of Systematic Bacteriology, 49: 1103-1109.
  • Dönmez, Y. (2014). Studies on vegetation geography of Turkey. İstanbul Üniversitesi Edebiyat Fakültesi Coğrafya Bölümü Coğrafya Dergisi, 29: 1-27.
  • Engin, M. S., Uyanık, A. & Cay, S. (2017). Investigation of trace metals distribution in water, sediments and wetland plants of Kızılırmak Delta, Turkey. International Journal of Sediment Research, 32: 90-97.
  • Eski, A., Demir, İ., Sezen, K. & Demirbağ, Z. (2017). A new biopesticide from a local Bacillus thuringiensis var. tenebrionis (Xd3) against alder leaf beetle (Coleoptera: Chrysomelidae). World Journal of Microbiology and Biotechnology, 33(5): 95. https://doi.org/10.1007/s11274-017-2263-0
  • Fayol-Messaoudi, D., Coconnier-Polter, M. H., Lievin-Le Moal, V., Atassi, F., Berger, C. N. & Servin, A. L. (2007). The Lactobacillus plantarum Strain ACA-DC287 isolated from a Greek cheese demonstrates antagonistic activity in vitro and in vivo against Salmonella enterica serovar typhimurium. Journal of Applied Microbiology, 103: 657-665.
  • Fedorova, T. V., Vasina, D. V., Begunova, A. V., Rozhkova, I. V., Raskoshnaya, T. A. & Gabrielyan, N. I. (2018). Antagonistic activity of lactic acid bacteria Lactobacillus spp. against clinical isolates of Klebsiella pneumonia. Applied Biochemistry & Microbiology, 54(3): 277-287.
  • Garbeva, P., van Veen, J. A. & van Elsas, J. D. (2003). Predominant Bacillus spp. in agricultural soil under different management regimes detected via PCR-DGGE. Microbial Ecology, 45: 302-316. https://doi.org/10.1007/s00248-002-2034-8
  • Gomez-Gil, B., Roque, A. & Turnbull, J. F. (2000). The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms. Aquaculture, 191: 259-270.
  • Gopal, P. K., Prasad, J., Smart, J. & Gill, H. S. (2001). In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. International Journal of Food Microbiology, 67: 207-216.
  • Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 95-98.
  • Heumann, W. (1960). Versuche zur Rekombination Sternbildender Bakterien. Naturwissenschaften, 47: 330-331.
  • İçgen, B. & Yılmaz, F. (2014). Co-occurrence of antibiotic and heavy metal resistance in Kızılırmak River isolates. Bulletin of Environmental Contamination and Toxicology, 93: 735-743.
  • Irkitova, A. N., Grebenshchikova, A. V. & Matsyura, A. V. (2018). Antagonistic activity of Bacillus subtilis strains isolated from various sources. Ukrainian Journal of Ecology, 8(2): 354-364.
  • Jeong, S. J., Heo, K., Park, J. Y., Lee, K. W., Park, J. Y., Joo, S. H. & Kim, J. H. (2015). Characterization of AprE176, a fibrinolytic enzyme from Bacillus subtilis HK176. Journal of Microbiology and Biotechnology, 25(1): 89-97.
  • Kan, N. İ. & Sarıeyyüpoğlu, M. (2008). Investigation of streptococci in fish caught from region of Elaziğ city sewage discharged into Keban Dam Lake. Fırat Üniversitesi Fen Bilimleri Dergisi, 20(2): 271-277. (In Turkish)
  • Katırcıoğlu, H. (2001). Gökkuşağı Alabalığı ve Aynalı Sazandan izole edilen laktik asit bakterilerinin metabolik ve antimikrobiyal aktivitelerinin incelenmesi. Gazi Üniversitesi Fen Bilimleri Enstitüsü Biyoloji Ana Bilim Dalı, Doktora tezi, 139, Ankara.
  • Kavuthodi, B. & Sebastian, D. (2018). Review on bacterial production of alkaline pectinase with special emphasis on Bacillus species. Bioscience Biotechnology Research Communications, 11(1): 18-30.
  • Kim, H.S., Lee, O. K., Lee, S. J., Hwang, S., Kim, S. J., Yang, S. H., Park, S. & Lee, E. Y. (2006). Enantioselective epoxide hydrolase activity of a newly isolated microorganism, Sphingomonas echinoides EH-983, from seawater. Journal of Molecular Catalysis B: Enzymatic, 41: 130-135. https://doi.org/10.1016/j.molcatb.2006.05.009
  • Kimura, S., Bryan, C. G., Hallberg, K. B. & Johnson, D. B. (2011). Biodiversity and geochemistry of an extremely Acidic, low-temperature subterranean environment sustained by chemolithotrophy. Environmental Microbiology, 13(8):2092–2104. https://doi.org/10.1111/j.1462-2920.2011.02434.x
  • Lane, D.J. (1991). 16S/23S rRNA sequencing. In: Nucleic Acid Techniques in Bacterial Systematics, Ed. E. Stackebrandt and M. Goodfellow. John Wiley and Sons, Chichester. 115-175.
  • Larkin, M. A., Blackshields, G., Brown, N., Chenna, R., Mcgettigan, P. A., Mcwilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & Lopez, R. (2007). Clustal W and Clustal X version 2.0. Bioinformatics. 23: 2947-2948.
  • Lee, M. J., Lee, J. J., Chung, H. Y., Choi, S. H. & Kim, B. S. (2016). Analysis of microbiota on abalone (Haliotis discus hannai) in South Korea for Improved product management. International Journal of Food Microbiology, 234: 45-52.
  • Li, Z., Bai, Z., Zhang, B., Xie, H., Hu, Q., Hao, C., Xue, W. & Zhang, H. (2005). Newly isolated Bacillus gibsonii S-2 Capable of using sugar beet pulp for alkaline pectinase production. World Journal of Microbiology & Biotechnology, 21: 1483-1486. https://doi.org/10.1007/s11274-005-7025-8
  • Logan, N. A. & De Vos, P. (2009). Genus: Bacillus, Bergey’s manual of systematics bacteriology Vol III, Springer Dordrecht Heidelberg London New York, 21-128.
  • Ma, Y. X., Li, L. Y., Bao, P. Y., Li, M., Chen, W. & Chang Y. Q. (2018). Effects of combined dietary administration of Rhodotorula sp. H26 and Bacillus sp. BC26 on growth, immunity and intestinal microbiota in juvenile Sea Cucumber, Apostichopus japonicus. Aquaculture Research, 49: 3792-3803.
  • Muz, A., Sarıeyyüpoğlu, M., Ertaş, H. B. & Şimşek, A. (1995). Keban Baraj Gölü’nden yakalanan bazı balıkların aerobik ve mikroaerofilik bakteriler yönünden incelenmesi. Fırat Üniversitesi Sağlık Bilimleri Dergisi, 9(2): 212-219.
  • Nannan, C., Vu, H. Q., Gillis, A., Gaulier, S., Nguyen, T. T. T. & Mahillon, J. (2021). Bacilysin within the Bacillus subtilis Group: Gene Prevalence versus antagonistic activity against Gram-negative foodborne pathogens. Journal of Biotechnology, 327: 28-35.
  • Orozova, P., Sirakov, I., Austin, D. A. & Austin, B. (2018). Recovery of Bacillus mycoides, B. pseudomycoides and Aeromonas hydrophila from common carp (Cyprinus carpio) and Rainbow Trout (Oncorhynchus mykiss) with gill disease. Journal of Fish Diseases, 41(1): 125-129.
  • Özer, G., Ergene, A. & İçgen, B. (2013). Biochemical and molecular characterization of strontium-resistant environmental isolates of Pseudomonas fluorescens and Sphingomonas paucimobilis. Geomicrobiology Journal, 30: 381-390. https://doi.org/10.1080/01490451.2012.694977
  • Özer, S., Demirel, M., Us, M. & Yıldırım, S. (2008). Microbial flora of rainbow trout (Oncorhynchus mykiss, Walbaum) hatcheries in Çağlarca, province Mersin-Turkey. Journal of FisheriesSciences.com, 2(3): 261-271. (In Turkish) https://doi.org/10.3153/jfscom.mug.200713
  • Öztürk, T., Didinen, B. I., Doğan, G., Özer, A. & Bircan, R. (2013). Lactococcosis in Rainbow Trout (Oncorhynchus mykiss, Walbaum, 1792) in the Middle Black Sea Region in Turkey and antimicrobial susceptibility of the aetiological agent, Lactococcus garvieae. Etlik Vet Mikrobiyol Derg, 24:7-12.
  • Pandey, A. K., Patel, A. K., Banjare, U. & Singh, R. K. (2021). Molecular characterization of bacterial microbiome isolated from wheat rhizosphere of agro climatic zones of India. Indian Journal of Natural Sciences, 12(67): 33033-33042.
  • Piccini, C., Conde, D., Alonso, C., Sommaruga, R. & Pernthalter, J. (2006). Blooms of single bacterial species in a coastal lagoon of the Southwestern Atlantic Ocean. Applied and Environmental Microbiology, 72(10): 6560–6568. https://doi.org/10.1128/AEM.01089-06
  • Rafat, A., Philip, K. & Muniandy, S. (2012). A novel source of bioactive compounds: Endophytic bacteria isolated from Centella asiatica. Journal of Pure and Applied Microbiology, 6(1): 11-20.
  • Ringo, E. & Gatesoupe, F. J. (1998). Lactic acid bacteria in fish: a review. Aquaculture, 160: 177-203.
  • Roberts, R. J. (2012). Fish pathology 4th edition, Wiley-Blackwell, UK.
  • Sezen, K., İşci, Ş., Muratoğlu, H., İnan, K. & Demirbağ, Z. (2013). Identification and pathogenicity of bacteria from Gryllotalpa gryllotalpa L. (Orthoptera: Gryllotalpidae). Türkiye Biyolojik Mücadele Dergisi, 4(2): 89-108.
  • Shin, S. C., Kim, S. J., Ahn, D. H., Lee, J. K. & Park, H. (2012). Draft genome sequence of Sphingomonas echinoides ATCC 14820. Journal of Bacteriology, 194(7): 1843.
  • Singh, B. R., Agrawal, R., Vadhana, P., Bhardwaj, M. & Dubey, S. (2015). Antimicrobial activity of citronella essential oil on antimicrobial drug resistant bacteria from veterinary clinical cases. Clinical & Medical Biochemistry, 1(1): 1000106.
  • Tambekar, D. H. & Dhundale, V. R. (2012). Studies on the physiological and cultural diversity of bacilli characterized from Lonar Lake (Ms) India. Bioscience Discovery, 3(1): 34-39.
  • Taş, B. (2006). Investigation of water quality of Derbent Dam Lake (Samsun). Ekoloji, 60:1-6.
  • TUIK (2020). Turkish Statistical Institute Retrieved on November 06, 2020 from https://tuikweb.tuik.gov.tr/PreTablo.do?alt_id=1005
  • Tuo, Y., Zhang, W., Zhang, L., Ai, L., Zhang, Y., Han, X. & Yi, H. (2013). Study of probiotic potential of four wild Lactobacillus rhamnosus strains. Anaerobe, 21: 22-27.
  • Türe, M., Altınok, İ., Işıdan, H., Savaş, H. & Kutlu, İ. (2012). PFGE metodu kullanılarak Lactoccoccus garvieae’nin genetik çeşitliliğinin ve yayılımının belirlenmesi, TAGEM Proje Sonuç Raporu. Su Ürünleri Merkez Araştırma Enstitüsü, Trabzon.
  • Verdenelli, M. C., Ghelfi, F., Silvi, S., Orpianesi, C., Cecchini, C. & Cresci, A. (2009). Probiotic properties of Lactobacillus rhamnosus and Lactobacillus paracasei isolated from human faeces. European Journal of Nutrition, 48: 355-363.
  • Wikler, M. (2006). Performance Standards for Antimicrobial Susceptibility Testing. Wayne, PA; Clinical and Laboratory Standards Insitute.
  • Yabuuchi, E. & Kosako, Y. (2005). Genus: Sphingomonas Bergey’s manual of systematics bacteriology Vol II part C, Springer Dordrecht Heidelberg London New York, 21-128.
  • Yuan, X., Zhou, Y., Liang, X.F., Guo, X., Fang, L., Li, J., Liu, L. & Li, B. (2015). Effect of dietary glutathione supplementation on the biological value of rapeseed meal to juvenile Grass Carp, Ctenopharyngodon idellus. Aquaculture Nutrition, 21: 73-84. https://doi.org/10.1111/anu.12142
  • Zhang, B., Fan, R., Bai, Z., Wang, S., Wang, L. & Shi, J. (2013). Biosorption characteristics of Bacillus gibsonii S-2 waste biomass for removal of lead (II) from aqueous solution. Environmental Science and Pollution Research, 20: 1367-1373. https://doi.org/10.1007/s11356-012-1146-z
  • Zhang, Z., Schwartz, S., Wagner, L. & Miller, W. (2000). A greedy algorithm for aligning DNA sequences. Journal of Computational Biology, 7: 203-214.
  • Zhou, Y., Yuan, X., Liang, X.F., Fang, L., Li, J., Guo, X., Bai, X. & He, S. (2013). Enhancement of growth and intestinal flora in Grass Carp: The Effect of exogenous cellulose. Aquaculture, 416-417: 1-7.
There are 70 citations in total.

Details

Primary Language English
Subjects Hydrobiology
Journal Section Research Articles
Authors

Özgür Çanak 0000-0001-6194-0096

Tülay Akaylı 0000-0003-2375-2224

Çiğdem Ürkü 0000-0003-0381-9321

Project Number FBA-28476
Publication Date December 31, 2021
Submission Date September 23, 2021
Acceptance Date October 30, 2021
Published in Issue Year 2021 Volume: 3 Issue: 2

Cite

APA Çanak, Ö., Akaylı, T., & Ürkü, Ç. (2021). A mixed Bacillus gibsonii and Sphingomonas echinoides infection in cultured rainbow trout (Oncorhynchus mykiss). Marine and Life Sciences, 3(2), 71-79. https://doi.org/10.51756/marlife.999539

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