Pathogenic profile and cytotoxic activity of Aeromonas spp. isolated from Pectinatella magnifica and surrounding water in the South Bohemian aquaculture region
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.1.01/0.0/0.0/16_019/0000845
European Regional Development Fund-Project NutRisk
20182020
Internal Grant Agency (CIGA) of the Czech University of Life Sciences Prague
PubMed
32776333
DOI
10.1111/jfd.13223
Knihovny.cz E-zdroje
- Klíčová slova
- Aeromonas, Pectinatella magnifica, cytotoxicity, pathogenicity, virulence factors,
- MeSH
- Aeromonas genetika patogenita MeSH
- bakteriální proteiny genetika MeSH
- Bryozoa mikrobiologie MeSH
- enterotoxiny genetika MeSH
- faktory virulence genetika MeSH
- sladká voda MeSH
- virulence MeSH
- vodní hospodářství MeSH
- zavlečené druhy MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Česká republika MeSH
- Názvy látek
- bakteriální proteiny MeSH
- enterotoxiny MeSH
- faktory virulence MeSH
Pectinatella magnifica is an invasive freshwater bryozoan that has expanded in many localities worldwide, including fishing areas. It contains microbial communities, predominantly consisting of Aeromonas bacteria that are frequently associated with fish infections. The objective of this study was to investigate the potential pathogenicity of Aeromonas spp. associated with P. magnifica and evaluate the health risks for fish. Aeromonas strains were isolated from P. magnifica (101 strains) and from surrounding water (29 strains) in the South Bohemian region and investigated for the presence of 14 virulence-associated genes using PCR. We demonstrated high prevalence of phospholipase GCAT, polar flagellin, enolase, DNAse, aerolysin/cytotoxic enterotoxin, serine protease and heat-stable cytotonic enterotoxin-coding genes. Further, all twelve isolates that were analysed for cytotoxicity against intestinal epithelial cells were found to be cytotoxic. Six of the isolates were also tested as co-cultures composed of pairs. Enhanced cytotoxicity was observed when the pair was composed of strains from different species. In conclusion, P. magnifica is colonized by Aeromonas strains that have a relatively high prevalence of virulence-associated genes and the ability to provoke disease. Results also suggest a possibly increased risk arising from mixed infections.
Zobrazit více v PubMed
Abrami, L., Fivaz, M., Decroly, E., Seidah, N. G., Jean, F., Thomas, G., … van der Goot, F. G. (1998). The pore-forming toxin proaerolysin is activated by furin. Journal of Biological Chemistry, 273(49), 32656-32661. https://doi.org/10.1074/jbc.273.49.32656
Abrami, L., Fivaz, M., Glauser, P. E., Sugimoto, N., Zurzolo, C., & Van der Goot, F. G. (2003). Sensitivity of polarized epithelial cells to the pore-forming toxin aerolysin. Infection and Immunity, 71(2), 739-746. https://doi.org/10.1128/IAI.71.2.739-746.2003
Adámek, Z., Linhart, O., Kratochvíl, M., Flajšhans, M., Randák, T., Policar, T., & Kozák, P. (2012). Aquaculture in the Czech Republic in 2012: Modern European prosperous sector based on thousand-year history of pond culture. Aquaculture Europe, 37(2), 5-14.
Alperi, A., & Figueras, M. J. (2010). Human isolates of Aeromonas possess Shiga toxin genes (stx1 and stx2) highly similar to the most virulent gene variants of Escherichia coli. Clinical Microbiology and Infection, 16(10), 1563-1567. https://doi.org/10.1111/j.1469-0691.2010.03203.x
Aoki, T., & Hirono, I. (1991). Cloning and characterization of the haemolysin determinants from Aeromonas hydrophila. Journal of Fish Diseases, 14(3), 303-312. https://doi.org/10.1111/j.1365-2761.1991.tb00827.x
Aravena-Román, M., Inglis, T. J. J., Riley, T. V., & Chang, B. J. (2014). Distribution of 13 virulence genes among clinical and environmental Aeromonas spp. in Western Australia. European Journal of Clinical Microbiology & Infectious Diseases, 33(11), 1889-1895. https://doi.org/10.1007/s10096-014-2157-0
Austin, B., & Austin, D. A. (2016). Aeromonadaceae representatives (motile aeromonads). In B. Austin, & D. A Austin (Eds.), Bacterial Fish Pathogens (pp. 161-214). Cham, CH: Springer International Publishing. https://doi.org/10.1007/978-3-319-32674-0_4
Bais, H. P., Fall, R., & Vivanco, M. (2013). Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: A review. Applied and Environmental Microbiology, 8(2), 274-302. https://doi.org/10.1104/pp.103.028712.zobacterium
Balounová, Z., Pechoušková, E., Rajchard, J., Joza, V., & Šinko, J. (2013). World-wide distribution of the bryozoan Pectinatella magnifica (Leidy 1851). European Journal of Environmental Sciences, 3(2), 96-100. https://doi.org/10.14712/23361964.2015.11
Balounová, Z., Rajchard, J., Švehla, J., & Šmahel, L. (2011). The onset of invasion of bryozoan Pectinatella magnifica in South Bohemia (Czech Republic). Biologia, 66(6), 1091-1096. https://doi.org/10.2478/s11756-011-0118-y
Beaz-Hidalgo, R., & Figueras, M. J. (2013). Aeromonas spp. whole genomes and virulence factors implicated in fish disease. Journal of Fish Diseases, 36(4), 371-388. https://doi.org/10.1111/jfd.12025
Brooks, C. M. (1929). Notes on the statoblasts and polypids of Pectinatella magnifica. Proceedings of the Academy of Natural Sciences of Philadelphia, 81, 427-441. https://www.jstor.org/stable/4064038?seq=1#page_scan_tab_contents
Buckley, J. T., Howard, S. P., Chopra, A. K., & Houston, C. W. (1999). The cytotoxic enterotoxin of Aeromonas hydrophila is aerolysin (multiple letters). Infection and Immunity, 67(1), 466-467.
Canning, E. U., Refardt, D., Vossbrinck, C. R., Okamura, B., & Curry, A. (2002). New diplokaryotic microsporidia (Phylum Microsporidia) from freshwater bryozoans (Bryozoa, Phylactolaemata). European Journal of Protistology, 38(3), 247-265. https://doi.org/10.1078/0932-4739-00867
Chacón, M. R., Castro-Escarpulli, G., Soler, L., Guarro, J., & Figueras, M. J. (2002). A DNA probe specific for Aeromonas colonies. Diagnostic Microbiology and Infectious Disease, 44(3), 221-225. https://doi.org/10.1016/S0732-8893(02)00455-8
Chacón, M. R., Figueras, M. J., Castro-Escarpulli, G., Soler, L., & Guarro, J. (2003). Distribution of virulence genes in clinical and environmental isolates of Aeromonas spp. Antonie Van Leeuwenhoek, 84(4), 269-278. https://doi.org/10.1023/A:1026042125243
Chacón, M. R., Soler, L., Groisman, E. A., Guarro, J., & Figueras, M. J. (2004). Type III secretion system genes in clinical Aeromonas isolates. Journal of Clinical Microbiology, 42(3), 1285-1287. https://doi.org/10.1128/jcm.42.3.1285-1287.2004
Chopra, A. K., Houston, C. W., Peterson, J. W., & Jin, G. F. (1993). Cloning, expression, and sequence analysis of a cytolytic enterotoxin gene from Aeromonas hydrophila. Canadian Journal of Microbiology, 39(5), 513-523. https://doi.org/10.1139/m93-073
Chopra, A. K., Xu, X. J., Ribardo, D., Gonzalez, M., Kuhl, K., Peterson, J. W., & Houston, C. W. (2000). The cytotoxic enterotoxin of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Infection and Immunity, 68(5), 2808-2818. https://doi.org/10.1128/IAI.68.5.2808-2818.2000
Chuang, Y. C., Chiou, S. F., Su, J. H., Wu, M. L., & Chang, M. C. (1997). Molecular analysis and expression of the extracellular lipase of Aeromonas hydrophila MCC-2. Microbiology, 143(3), 803-812. https://doi.org/10.1099/00221287-143-3-803
Cocito, S. (2004). Bioconstruction and biodiversity: Their mutual influence. Scientia Marina, 68(1), 137-144. https://doi.org/10.3989/scimar.2004.68s1137
Crumlish, M., Thanh, P. C., Koesling, J., Tung, V. T., & Gravningen, K. (2010). Experimental challenge studies in Vietnamese catfish, Pangasianodon hypophthalmus (Sauvage), exposed to Edwardsiella ictaluri and Aeromonas hydrophila. Journal of Fish Diseases, 33(9), 717-722. https://doi.org/10.1111/j.1365-2761.2010.01173.x
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(1-2), 1-7. https://doi.org/10.1016/j.vetmic.2013.06.025
Dong, H. T., Techatanakitarnan, C., Jindakittikul, P., Thaiprayoon, A., Taengphu, S., Charoensapsri, W., … Senapin, S. (2017). Aeromonas jandaei and Aeromonas veronii caused disease and mortality in Nile tilapia, Oreochromis niloticus (L.). Journal of Fish Diseases, 40(10), 1395-1403. https://doi.org/10.1111/jfd.12617
Fivaz, M., Abrami, L., Tsitrin, Y., & van der Goot, F. G. (2000). Aerolysin from Aeromonas hydrophila and related toxins. In F. G. van der Goot (Eds), Pore-Forming Toxins Current Topics in Microbiology and Immunology (pp. 35-52). Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-642-56508-3_3
Gavín, R., Merino, S., Altarriba, M., Canals, R., Shaw, J. G., & Tomás, J. M. (2003). Lateral flagella are required for increased cell adherence, invasion and biofilm formation by Aeromonas spp. FEMS Microbiology Letters, 224(1), 77-83. https://doi.org/10.1016/S0378-1097(03)00418-X
Gonzalez-Serrano, C. J., Santos, J. A., Garcia-Lopez, M. L., & Otero, A. (2002). Virulence markers in Aeromonas hydrophila and Aeromonas veronii biovar sobria isolates from freshwater fish and from a diarrhoea case. Journal of Applied Microbiology, 93(3), 414-419. https://doi.org/10.1046/j.1365-2672.2002.01705.x
Imamura, T., Nitta, H., Wada, Y., Kobayashi, H., & Okamoto, K. (2008). Impaired plasma clottability induction through fibrinogen degradation by ASP, a serine protease released from Aeromonas sobria. FEMS Microbiology Letters, 284(1), 35-42. https://doi.org/10.1111/j.1574-6968.2008.01184.x
Ingold, J. L., Mundahl, N. D., Weigt, L. A., & Guttman, S. I. (1984). Ecology and population genetics of the freshwater bryozoan, Pectinatella magnifica Leidy. Journal of Freshwater Ecology, 2(5), 499-508. https://doi.org/10.1080/02705060.1984.9664630
Janda, J. M., & Abbott, S. L. (2010). The genus Aeromonas: Taxonomy, pathogenicity, and infection. Clinical Microbiology Reviews, 23(1), 35-73. https://doi.org/10.1128/CMR.00039-09
Jawahar Abraham, T., Sarker, S., Dash, G., Patra, A., & Adikesavalu, H. (2017). Chryseobacterium sp. PLI2 and Aeromonas hydrophila co-infection in pacu, Piaractus brachypomus (Cuvier, 1817) fries cultured in West Bengal, India. Aquaculture, 473, 223-227. https://doi.org/10.1016/j.aquaculture.2017.02.016
Joo, G.-J., Ward, A. K., & Ward, G. M. (1992). Ecology of Pectinatella magnifica (Bryozoa) in an Alabama oxbow lake: Colony growth and association with algae. Journal of the North American Benthological Society, 11(3), 324-333. https://doi.org/10.2307/1467652
Khor, W. C., Puah, S. M., Tan, J. A., Puthucheary, S. D., & Chua, K. H. (2015). Phenotypic and genetic diversity of Aeromonas species isolated from fresh water lakes in Malaysia. PLoS One, 10(12), e0145933. https://doi.org/10.1371/journal.pone.0145933
Kingombe, C. I., Huys, G., Tonolla, M., Albert, M. J., Swings, J., Peduzzi, R., & Jemmi, T. (1999). PCR detection, characterization, and distribution of virulence genes in Aeromonas spp. Applied and Environmental Microbiology, 65(12), 5293-5302. https://doi.org/10.1128/AEM.65.12.5293-5302.1999
Kirov, S. M., Castrisios, M., & Shaw, J. G. (2004). Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces. Infection and Immunity, 72(4), 1939-1945. https://doi.org/10.1128/iai.72.4.1939-1945.2004
Ko, E. J., Gim, J. S., Hong, S., Jo, H., Kim, J. Y., Hirose, M., … Joo, G. J. (2019). Distribution and growth of non-native bryozoan Pectinatella magnifica (Leidy, 1851) in four large rivers in South Korea. Aquatic Invasions, 14(2), 384-396. https://doi.org/10.3391/ai.2019.14.2.14
Kobayashi, H., Seike, S., Yamaguchi, M., Ueda, M., Takahashi, E., Okamoto, K., & Yamanaka, H. (2019). Aeromonas sobria serine protease decreases epithelial barrier function in T84 cells and accelerates bacterial translocation across the T84 monolayer in vitro. PLoS One, 14(8), e0221344. https://doi.org/10.1371/journal.pone.0221344
Kollar, P., Šmejkal, K., Salmonová, H., Vlková, E., Lepšová-Skácelová, O., Balounová, Z., … Pazourek, J. (2016). Assessment of chemical impact of invasive bryozoan Pectinatella magnifica on the environment: Cytotoxicity and antimicrobial activity of P. magnifica extracts. Molecules, 21(11), e1476. https://doi.org/10.3390/molecules21111476
Kotob, M. H., Menanteau-Ledouble, S., Kumar, G., Abdelzaher, M., & El-Matbouli, M. (2016). The impact of co-infections on fish: A review. Veterinary Research, 47, 98. https://doi.org/10.1186/s13567-016-0383-4
Kozińska, A. (2007). Dominant pathogenic species of mesophilic aeromonads isolated from diseased and healthy fish cultured in Poland. Journal of Fish Diseases, 30(5), 293-301. https://doi.org/10.1111/j.1365-2761.2007.00813.x
Lidgard, S. (2008). Predation on marine bryozoan colonies: Taxa, traits and trophic groups. Marine Ecology Progress Series, 359, 117-131. https://doi.org/10.3354/meps07322
Martin-Carnahan, A., & Joseph, S. W. (2015). Aeromonas. In W. B. Whitman, F. Rainey, P. Kämpfer, M. Trujillo, J. Chun, P. DeVos, B. Hedlund, & S. Dedysh (Eds.), Bergey's Manual of Systematics of Archaea and Bacteria (pp. 1-44). Hoboken, NJ: John Wiley & Sons, Ltd. https://doi.org/10.1002/9781118960608.gbm01081
Massard, J. A., & Geimer, G. (2008). Global diversity of bryozoans (Bryozoa or Ectoprocta) in freshwater. Hydrobiologia, 595(1), 93-99. https://doi.org/10.1007/s10750-007-9007-3
Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65(1-2), 55-63. https://doi.org/10.1016/0022-1759(83)90303-4
Mosser, T., Talagrand-Reboul, E., Colston, S. M., Graf, J., Figueras, M. J., Jumas-Bilak, E., & Lamy, B. (2015). Exposure to pairs of Aeromonas strains enhances virulence in the Caenorhabditis elegans infection model. Frontiers in Microbiology, 6, 1-14. https://doi.org/10.3389/fmicb.2015.01218
Mota, L. J., & Cornelis, G. R. (2005). The bacterial injection kit: Type III secretion systems. Annals of Medicine, 37(4), 234-249. https://doi.org/10.1080/07853890510037329
Newton, R. J., Jones, S. E., Eiler, A., McMahon, K. D., & Bertilsson, S. (2011). A Guide to the natural history of freshwater lake bacteria. Microbiology and Molecular Biology Reviews, 75(1), 14-49. https://doi.org/10.1128/mmbr.00028-10
Nusbaum, K. E., & Morrison, E. E. (2002). Edwardsiella ictaluri bacteraemia elicits shedding of Aeromonas hydrophila complex in latently infected channel catfish, Ictalurus punctatus (Rafinesque). Journal of Fish Diseases, 25(6), 343-350. https://doi.org/10.1046/j.1365-2761.2002.00379.x
Perretta, A., Antúnez, K., & Zunino, P. (2018). Phenotypic, molecular and pathological characterization of motile aeromonads isolated from diseased fishes cultured in Uruguay. Journal of Fish Diseases, 41(10), 1559-1569. https://doi.org/10.1111/jfd.12864
Preston, G. M. (2007). Metropolitan microbes: Type III secretion in multihost symbionts. Cell Host and Microbe, 2(5), 291-294. https://doi.org/10.1016/j.chom.2007.10.004
Rahman, M., Colque-Navarro, P., Kühn, I., Huys, G., Swings, J., & Möllby, R. (2002). Identification and characterization of pathogenic Aeromonas veronii biovar sobria associated with epizootic ulcerative syndrome in fish in Bangladesh. Applied and Environmental Microbiology, 68(2), 650-655. https://doi.org/10.1128/AEM.68.2.650-655.2002
Ran, C., Qin, C., Xie, M., Zhang, J., Li, J., Xie, Y., … Zhou, Z. (2018). Aeromonas veronii and aerolysin are important for the pathogenesis of motile aeromonad septicemia in cyprinid fish. Environmental Microbiology, 20(9), 3442-3456. https://doi.org/10.1111/1462-2920.14390
Rasmussen-Ivey, C. R., Figueras, M. J., McGarey, D., & Liles, M. R. (2016). Virulence factors of Aeromonas hydrophila: In the wake of reclassification. Frontiers in Microbiology, 7, 1337. https://doi.org/10.3389/fmicb.2016.01337
Rather, M. A., Willayat, M. M., Wani, S. A., Hussain, S. A., & Shah, S. A. (2019). Enterotoxin gene profile and molecular epidemiology of Aeromonas species from fish and diverse water sources. Journal of Applied Microbiology, 127(3), 921-931. https://doi.org/10.1111/jam.14351
Rather, M. A., Willayat, M. M., Wani, S. A., Munshi, Z. H., & Hussain, S. A. (2014). A multiplex PCR for detection of enterotoxin genes in Aeromonas species isolated from foods of animal origin and human diarrhoeal samples. Journal of Applied Microbiology, 117(6), 1721-1729. https://doi.org/10.1111/jam.12641
Salmonová, H., Killer, J., Bunešová, V., Geigerová, M., & Vlková, E. (2018). Cultivable bacteria from Pectinatella magnifica and the surrounding water in South Bohemia indicate potential new Gammaproteobacterial, Betaproteobacterial and Firmicutes taxa. FEMS Microbiology Letters, 365(13), fny118. https://doi.org/10.1093/femsle/fny118
Santos, P. G., Santos, P. A., Bello, A. R., & Freitas-Almeida, A. C. (2011). Association of Aeromonas caviae polar and lateral flagella with biofilm formation. Letters in Applied Microbiology, 52(1), 49-55. https://doi.org/10.1111/j.1472-765X.2010.02965.x
Sen, K., & Rodgers, M. (2004). Distribution of six virulence factors in Aeromonas species isolated from US drinking water utilities: A PCR identification. Journal of Applied Microbiology, 97(5), 1077-1086. https://doi.org/10.1111/j.1365-2672.2004.02398.x
Šetlíková, I., Skácelová, O., Šinko, J., Rajchard, J., & Balounová, Z. (2013). Ecology of Pectinatella magnifica and associated algae and cyanobacteria. Biologia, 68(6), 1136-1141. https://doi.org/10.2478/s11756-013-0262-7
Sha, J., Erova, T. E., Alyea, R. A., Wang, S., Olano, J. P., Pancholi, V., & Chopra, A. K. (2009). Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophilaa. Journal of Bacteriology, 191(9), 3095-3107. https://doi.org/10.1128/JB.00005-09
Sha, J., Galindo, C. L., Pancholi, V., Popov, V. L., Zhao, Y., Houston, C. W., & Chopra, A. K. (2003). Differential expression of the enolase gene under in vivo versus in vitro growth conditions of Aeromonas hydrophila. Microbial Pathogenesis, 34(4), 195-204. https://doi.org/10.1016/S0882-4010(03)00028-7
Sha, J., Kozlova, E. V., & Chopra, A. K. (2002). Role of various enterotoxins in Aeromonas hydrophila-induced gastroenteritis: Generation of enterotoxin gene-deficient mutants and evaluation of their enterotoxic activity. Infection and Immunity, 70(4), 1924-1935. https://doi.org/10.1128/IAI.70.4.1924-1935.2002
Silver, A. C., Williams, D., Faucher, J., Horneman, A. J., Gogarten, J. P., & Graf, J. (2011). Complex evolutionary history of the Aeromonas veronii group revealed by host interaction and DNA Sequence Data. PLoS One, 6(2), e16751. https://doi.org/10.1371/journal.pone.0016751
Soler, L., Figueras, M. J., Chacón, M. R., Vila, J., Marco, F., Martinez-Murcia, A. J., & Guarro, J. (2002). Potential virulence and antimicrobial susceptibility of Aeromonas popoffii recovered from freshwater and seawater. FEMS Immunology and Medical Microbiology, 32(3), 243-247. https://doi.org/10.1016/S0928-8244(01)00303-0
Syrova, E., Kohoutova, L., Dolejska, M., Papezikova, I., Kutilova, I., Cizek, A., … Palikova, M. (2018). Antibiotic resistance and virulence factors in mesophilic Aeromonas spp. from Czech carp fisheries. Journal of Applied Microbiology, 125(6), 1702-1713. https://doi.org/10.1111/jam.14075
Talagrand-Reboul, E., Latif-Eugenín, F., Beaz-Hidalgo, R., Colston, S., Figueras, M. J., Graf, J., … Lamy, B. (2018). Genome-driven evaluation and redesign of PCR tools for improving the detection of virulence-associated genes in aeromonads. PLoS One, 13(8), 1-17. https://doi.org/10.1371/journal.pone.0201428
Vilches, S., Jimenez, N., Tomás, J. M., & Merino, S. (2009). Aeromonas hydrophila AH-3 type III secretion system expression and regulatory network. Applied and Environmental Microbiology, 75(19), 6382-6392. https://doi.org/10.1128/AEM.00222-09
Vilches, S., Urgell, C., Merino, S., Chacón, M. R., Soler, L., Castro-escarpulli, G., … Tomás, J. M. (2004). Complete Type III secretion system of a mesophilic. Society, 70(11), 6914-6919. https://doi.org/10.1128/AEM.70.11.6914
Vipond, R., Bricknell, I. R., Durant, E., Bowden, T. J., Ellis, A. E., Smith, M., & MacIntyre, S. (1998). Defined deletion mutants demonstrate that the major secreted toxins are not essential for the virulence of Aeromonas salmonicida. Infection and Immunity, 66(5), 1990-1998. https://doi.org/10.1128/IAI.66.5.1990-1998.1998
Wahli, T., Burr, S. E., Pugovkin, D., Mueller, O., & Frey, J. (2005). Aeromonas sobria, a causative agent of disease in farmed perch, Perca fluviatilis L. Journal of Fish Diseases, 28(3), 141-150. https://doi.org/10.1111/j.1365-2761.2005.00608.x
Wang, B., Wang, H., & Cui, Y. (2017). Pectinatella magnifica (Leidy, 1851) (Bryozoa, Phylactolaemata), a biofouling bryozoan recently introduced to China. Chinese Journal of Oceanology and Limnology, 35(4), 815-820. https://doi.org/10.1007/s00343-017-6052-2
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(1), 65-71. https://doi.org/10.1111/j.1574-6968.1992.tb05543.x
Wood, T. S. (2010). Bryozoans. In J. H. Thorp, & A. P. Covich (Eds.), Ecology and Classification of North American Freshwater Invertebrates (3rd ed., pp. 437-454). Cambridge, MA: Academic Press. https://doi.org/10.1016/B978-0-12-374855-3.00013-3
Xiong, W., Sun, Y., Zhang, T., Ding, X., Li, Y., Wang, M., & Zeng, Z. (2015). Antibiotics, antibiotic resistance genes, and bacterial community composition in fresh water aquaculture environment in China. Microbial Ecology, 70(2), 425-432. https://doi.org/10.1007/s00248-015-0583-x
Zorić, K., Szekeres, J., Csányi, B., Kolarević, S., Marković, V., & Paunović, M. (2015). Distribution of the non-native bryozoan Pectinatella magnifica (Leidy, 1851) in the Danube river. Acta Zoologica Bulgarica, 67(2), 241-247.