Abstract
Aeromonas salmonicida is the typical pathogen causing furunculosis, reported widely in salmonids. Because of multiple serotypes, the control of A. salmonicida-caused disease has increasingly received much attention. Recently, A. salmonicida infection was reported in non-salmonid fish species. Here, a pathogenic A. salmonicida, named as As-s, was isolated from cultured snakehead (Channa argus) in a local fish farm in Shandong, China. As-s displayed clear hemolysis, amylase, and positive catalase activities, and grew at a wide range of temperatures (10-37 °C) and pH values (5.5-8.5). As-s was highly sensitive to cefuroxime sodium, ceftriaxone, ceftazidime, piperacillin, and cefoperazone and also apparently sensitive to chloramphenicol, erythromycin, and 25% cinnamaldehyde. The Virulence array protein gene cloning’ results suggested that As-s has this gene compared with the other two vapA-containing strains, despite a close relationship of these strains via phylogenetic analysis. Severe ulcers on skin, muscle, and abnormal liver, and hemorrhage in pectoral/ventral fins and anal region were observed, and exophthalmos were also noticed in infected juvenile snakehead, as well as necrosis and infiltration of blood cells emerged in the internal organs using pathological section. In addition, As-s caused high mortality in snakehead, consistently with its immune gene response. This study reports the first isolation of vapA-absent A. salmonicida in snakehead.
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References
Alghabshi A, Austin B, Crumlish M (2018) Aeromonas salmonicida isolated from wild and farmed fish and invertebrates in Oman. Int Aquat Res 10:145. https://doi.org/10.1007/s40071-018-0195-4
Aliyu-Paiko M, Hashim R, Shu-Chien AC (2010) Influence of dietary lipid/protein ratio on survival, growth, body indices and digestive lipase activity in snakehead (Channa striatus, Bloch 1793) fry reared in re-circulating water system. Aquac Nutr 16:466. https://doi.org/10.1111/j.1365-2095.2009.00683.x
Al-Mokaddem AK, Abdel-moneam DA, Ibrahim RA, Saleh M, Shaalan M (2022) Molecular identification, histopathological analysis and immunohistochemical characterization of non-pigmented Aeromonas salmonicida subsp. salmonicida in Mugil carinatus (Valenciennes, 1836). Aquac Rep 24:101103. https://doi.org/10.1016/j.aqrep.2022.101103
Austin B, Austin DA (2007) Bacterial fish pathogens: disease of farmed and wild fish, 4th edn. Praxis Publishing Ltd, Chichester, UK, pp 49–53, 186–199. https://doi.org/10.1007/978-1-4020-6069-4
Austin B, Austin DA (2016) Aeromonadaceae representative (Aeromonas salmonicida). In: Austin B, Austin DA (eds) Bacterial fish pathogens: disease of farmed and wild fish. Springer International Publishing, Cham, pp 215–321. https://doi.org/10.1007/978-94-007-4884-25
Austin D, McIntosh D, Austin B (1989) Taxonomy of fish associated Aeromonas spp., with the description of Aeromonas salmonicida subsp. Smithia subsp. nov. Syst Appl Microbiol 11:277. https://doi.org/10.1016/S0723-2020(89)80026-8
Bernoth EM (1997) 1-furunculosis: the history of the disease and of disease research. In: Bernoth E-M, Ellis AE, Midtlyng PJ, Olivier G, Smith P (eds) Furunculosis. Academic Press, San Diego, pp 1–20
Bhat RAH, Thakuria D, Dubey MK, Tandel RS, Sharma P, Khangembam VC, Dash P, Tripathi G, Sarman D (2021) Lethal dose and histopathological alterations induced by Aeromonas salmonicida in experimentally challenged common carp, Cyprinus carpio. Microb Pathog 158:105110. https://doi.org/10.1016/j.micpath.2021.105110
Bora A, Seervi KL, Solanki AN, Chandora AK, Meena SL, Chandora A, Rathore L, Daila M (2016) Isolation of Aeromonas salmonicida from human blood sample: a case report. J Clin Diagn Res 5:57–61. https://doi.org/10.20546/ijcmas.2016.503.008
Brietzke A, Korytář T, Jaros J, Köllner B, Goldammer T, Seyfert HM, Rebl A (2015) Aeromonas salmonicida infection only moderately regulates expression of factors contributing to Toll-Like receptor signaling but massively activates the cellular and humoral branches of innate immunity in rainbow trout (Oncorhynchus mykiss). J Immunol Res 2015:901015. https://doi.org/10.1155/2015/901015
Burr SE, Wahli T, Segner H, Pugovkin D, Frey J (2003) Association of type III secretion genes with virulence of Aeromonas salmonicida subsp. salmonicida. Dis Aquat Org 57:167. https://doi.org/10.3354/dao057167
Chen YF, Liang RS, Zhuo XL, Wu XT, Zou JX (2012) Isolation and characterization of Aeromonas schubertii from diseased snakehead, Channa maculata (Lacepède). J Fish Dis 35:421. https://doi.org/10.1111/j.1365-2761.2012.01362.x
Chu S, Feutrier CJ, Phipps BM, Kostrzynska M, Kay WW, Trust TJ (1991) Structure of the tetragonal surface virulence array protein and gene of Aeromonas salmonicida. J Biol Chem 266:15258. https://doi.org/10.1016/S0021-9258(18)98611-4
Courtenay WR, Williams JD (2004) Snakeheads: a biological synopsis and risk assessment, vol 1251. US Geological Survey. https://doi.org/10.3133/cir1251
Dallaire-Dufresne S, Barbeau X, Sarty D, Tanaka KH, Denoncourt AM, Lagüe P, Reith ME, Charette SJ (2013) Aeromonas salmonicida Ati2 is an effector protein of the type three secretion system. Microbiology 159:1937. https://doi.org/10.1099/mic.0.067959-0
Densmore CL, Iwanowicz LR, Henderson AP, Iwanowicz DD, Odenkirk JS (2016) Mycobacterial infection in Northern snakehead (Channa argus) from the Potomac River catchment. J Fish Dis 39:771–775. https://doi.org/10.1111/jfd.12412
Diamanka A, Loch TP, Cipriano RC, Winters AD, Faisal M (2014) Infection of sea lamprey with an unusual strain of Aeromonas salmonicida. J Wildl Dis 50:159. https://doi.org/10.7589/2013-01-026
Du X, Bayliss SC, Feil EJ, Liu Y, Wang C, Zhang G, Zhou D, Wei D, Tang N, Leclercq SO, Feng J (2019) Real time monitoring of Aeromonas salmonicida evolution in response to successive antibiotic therapies in a commercial fish farm. Environ Microbiol 21:1113. https://doi.org/10.1111/1462-2920.14531
Fang H, Xie J, Liao S, Guo T, Xie S, Liu Y, Tian L, Niu J (2019) Effects of dietary inclusion of shrimp paste on growth performance, digestive enzymes activities, antioxidant and immunological status and intestinal morphology of Hybrid Snakehead (Channa maculata ♀ × Channa argus ♂). Front Physiol 10:1027. https://doi.org/10.3389/fphys.2019.01027
Feng S, Su J, Lin L, Tu J (2019) Development of a reverse genetics system for snakehead vesiculovirus (SHVV). Virology 526:32. https://doi.org/10.1016/j.virol.2018.10.002
Fernández-Álvarez C, Gijón D, Álvarez M, Santos Y (2016) First isolation of Aeromonas salmonicida subspecies salmonicida from diseased sea bass, Dicentrarchus labrax (L.), cultured in Spain. Aquac Rep 4:36. https://doi.org/10.1016/j.aqrep.2016.05.006
Fu Y, Shi Z, Wu M, Zhang J, Jia L, Chen X (2011) Identification and differential expression of microRNAs during metamorphosis of the Japanese flounder (Paralichthys olivaceus). PLoS One 6(7):e22957. https://doi.org/10.1371/journal.pone.0022957
Glass ML, Ishimatsu A, Johansen K (1986) Responses of aerial ventilation to hypoxia and hypercapnia in Channa argus, an air-breathing fish. J Comp Physiol B Biochem Syst Environ Physiol 156:425. https://doi.org/10.1007/BF01101105
Groman D, Tweedie D, Shaw D (1992) Experiences with atypical furunculosis in Newfoundland: an overview. Bulletin of the AAC 1:36
Gudmundsdóttir S, Lange S, Magnadóttir B, Gudmundsdóttir BK (2003) Protection against atypical furunculosis in Atlantic halibut, Hippoglossus hippoglossus (L.); comparison of a commercial furunculosis vaccine and an autogenous vaccine. J Fish Dis 26:331. https://doi.org/10.1046/j.1365-2761.2003.00462.x
Gulla S, Lund V, Kristoffersen AB, Sørum H, Colquhoun DJ (2016) VapA (A-layer) typing differentiates Aeromonas salmonicida subspecies and identifies a number of previously undescribed subtypes. J Fish Dis 39:329. https://doi.org/10.1111/jfd.12367
Holt JG, Krieg NR, Sneath PH, Staley JT, Williams ST (1994) Bergey's manual of determinative bacteriology, 9th edn. William Wilkins
Jin S, Fu S, Li R, Dang H, Gao D, Ye S, Jiang Z (2020) Identification and histopathological and pathogenicity analysis of Aeromonas salmonicida from goldfish (Carassius auratus) in North China. AAF 5:36. https://doi.org/10.1016/j.aaf.2019.04.004
Kay WW, Buckley JT, Ishiguro EE, Phipps BM, Monette JP, Trust TJ (1981) Purification and disposition of a surface protein associated with virulence of Aeromonas salmonicida. J Bacteriol 147:1077. https://doi.org/10.1128/jb.147.3.1077-1084.1981
Kimura T (1969a) A new subspecies of Aeromonas salmonicida as an etiological agent of furunculosis on “Sakuramasu” (Oncorhynchus masou) and pink salmon (O. gorbuscha) rearing for maturity. Part 1.On the morphological and physiological properties. Fish Pathol 3:34. https://doi.org/10.3147/jsfp.3.2_45
Kimura T (1969b) A new subspecies of Aeromonas salmonicida as an etiological agent of furunculosis on “Sakuramasu” (Oncorhynchus masou) and pink salmon (O. gorbuscha) rearing for maturity. Part 2 on the serological properties. Fish Pathol 3:45. https://doi.org/10.3147/jsfp.3.2_45
Kong Y, Li M, Shan X, Wang G, Han G (2021) Effects of deltamethrin subacute exposure in snakehead fish, Channa argus: biochemicals, antioxidants and immune responses. Ecotoxicol Environ Saf 209:111821. https://doi.org/10.1016/j.ecoenv.2020.111821
Lee PG, Ng PK (2004) The systematics and ecology of snakeheads (Pisces: Channidae) in Peninsular Malaysia and Singapore. Hydrobiologia 285:59. https://doi.org/10.1007/BF00005654
Lehmann KB, Neumann RO (1896) Atlas und grundriss der bakteri ologie und lehrbuch der speziellen bakteriologischen diagnostik, vol 1. Lehmann. https://doi.org/10.5962/bhl.title.113833
Li Y, Lv X, Zhou J, Shi C, Duan T, Luo Y (2017) Does air-breathing meet metabolic demands of the juvenile snakehead, Channa argus, in multiple conditions. Biol Open 6:642. https://doi.org/10.1242/bio.024448
Lian Z, Bai J, Hu X, Lü A, Sun J, Guo Y, Song Y (2020) Detection and characterization of Aeromonas salmonicida subsp. salmonicida infection in crucian carp Carassius auratus. Vet Res Commun 44:61. https://doi.org/10.1007/s11259-020-09773-0
Liu J, Cui Y, Liu J (2000) Resting metabolism and heat increment of feeding in mandarin fish (Siniperca chuatsi) and Chinese snakehead (Channa argus). Comp Biochem Phys A 127:131. https://doi.org/10.1016/s1095-6433(00)00246-4
Liu JY, Li AH (2012) First case of Aeromonas schubertii infection in the freshwater cultured snakehead fish, Ophiocephalus argus (Cantor), in China. J Fish Dis 35:335. https://doi.org/10.1111/j.1365-2761.2012.01350.x
Liu S, Wang D, Cao Y, Lu T, Liu H, Li S (2020) Effects of propolis on the immune enhancement of the formalin-inactivated Aeromonas salmonicida vaccine. Aquac Res 51:4759. https://doi.org/10.1111/are.14822
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lowry R, Balboa S, Parker JL, Shaw JG (2014) Aeromonas flagella and colonisation mechanisms. Adv Microb Physiol 65:203. https://doi.org/10.1016/bs.ampbs.2014.08.007
Lü AJ, Wang RX, Hu XC, Sun JF, Li L, Pei C, Zhang C, Nie GX (2017) First report of Rahnella aquatilis infection in crucian carp Carassius auratus in China. Dis Aquat Org 123:205. https://doi.org/10.3354/dao03099
Marana MH, Skov J, Chettri JK, Krossøy B, Dalsgaard I, Kania PW, Buchmann K (2017) Positive correlation between Aeromonas salmonicida vaccine antigen concentration and protection in vaccinated rainbow trout Oncorhynchus mykiss evaluated by a tail fin infection model. J Fish Dis 40:507. https://doi.org/10.1111/jfd.12527
Massicotte MA, Vincent AT, Schneider A, Paquet VE, Frenette M, Charette SJ (2019) One Aeromonas salmonicida subsp. salmonicida isolate with a pAsa5 variant bearing antibiotic resistance and a pRAS3 variant making a link with a swine pathogen. Sci Total Environ 690:313. https://doi.org/10.1016/j.scitotenv.2019.06.456
McCarthy DH, Roberts RJ (1980) Furunculosis of fish–the present state of our knowledge. In: Droop MR, McCarthy DH, Jannasch HW (eds) Advances in aquatic microbiology. Academic Press, London, p 293
Menanteau-Ledouble S, Kumar G, Saleh M, El-Matbouli M (2016) Aeromonas salmonicida: updates on an old acquaintance. Dis Aquat Org 120:49. https://doi.org/10.3354/dao03006
Merino S, Aguilar A, Rubires X, Simon-Pujol D, Congregado F, Tomás JM (1996) The role of the capsular polysaccharide of Aeromonas salmonicida in the adherence and invasion of fish cell lines. FEMS Microbiol Lett 142:185. https://doi.org/10.1111/j.1574-6968.1996.tb08428.x
Nguyen TC, Li YC, Makouloutou P, Jimenez LA, Sato H (2012) Posthodiplostomum sp. Metacercariae in the trunk muscle of northern snakeheads (Channa argus) from the Fushinogawa River, Yamaguchi, Japan. J Vet Med Sci 74:1367. https://doi.org/10.1292/jvms.12-0025
Noga EJ (2013) Fish disease: Diagnosis and treatment, 2nd edn. Wiley-Blackwell. Print ISBN 9780813806976. Online ISBN:9781118786758, Ames, IA. https://doi.org/10.1002/9781118786758
Noonan B, Trust TJ (1995) Molecular analysis of an A-protein secretion mutant of Aeromonas salmonicida reveals a surface layer-specific protein secretion pathway. J Mol Biol 248:316. https://doi.org/10.1016/s0022-2836(95)80053-0
Ojala O (1966) Isolation of an anaerogenic bacterium resembling Aeromonas salmonicida in spawning lake trouts. Bull Off Int Epizoot 65:793 http://europepmc.org/abstract/MED/6007060
Papadopoulou A, Davie A, Monaghan SJ, Migaud H, Adams A (2021) Development of diagnostic assays for differentiation of atypical Aeromonas salmonicida vapA type V and type VI in ballan wrasse (Labrus bergylta, Ascanius). J Fish Dis 44:711. https://doi.org/10.1111/jfd.13334
Paterson WD, Douey D, Desautels D (1980) Isolation and identification of an atypical Aeromonas salmonicida strain causing epizootic losses among Atlantic salmon (Salmo salar)reared in a Nova Scotian hatchery. Can J Fish Aquat Sci 37:2236. https://doi.org/10.1139/f80-268
Pavan ME, Abbott SL, Zorzópulos J, Janda JM (2000) Aeromonas salmonicida subsp. pectinolytica subsp. nov., a new pectinase-positive subspecies isolated from a heavily polluted river. Int J Syst Evol Microbiol 50:1119. https://doi.org/10.1099/00207713-50-3-1119
Rajendiran AS, Natarajan E, Subramanian P (2008) Control of Aeromonas hydrophila infection in spotted snakehead, Channa punctatus, by Solanum nigrum L., a Medicinal Plant. J World Aquacult Soc 39:375. https://doi.org/10.1111/j.1749-7345.2008.00163.x
Resh CA, Galaska MP, Mahon AR (2018) Genomic analyses of Northern snakehead (Channa argus) populations in North America. Peer J 6:e4581. https://doi.org/10.7717/peerj.4581
Rintamäki P, Valtonen ET (1991) Aeromonas salmonicida in Finland: pathological problems associated with atypical and typical strains. J Fish Dis 14:323. https://doi.org/10.1111/j.1365-2761.1991.tb00829.x
Rouleau FD, Vincent AT, Charette SJ (2018) Genomic and phenotypic characterization of an atypical Aeromonas salmonicida strain isolated from a lumpfish and producing unusual granular structures. J Fish Dis 41:673. https://doi.org/10.1111/jfd.12769
Rupp M, Pilo P, Müller B, Knüsel R, von Siebenthal B, Frey J, Sindilariu PD, Schmidt-Posthaus H (2019) Systemic infection in European perch with thermoadapted virulent Aeromonas salmonicida (Perca fluviatilis). J Fish Dis 42:685. https://doi.org/10.1111/jfd.12970
Sagada G, Chen J, Shen B, Huang A, Sun L, Jiang J, Jin C (2017) Optimizing protein and lipid levels in practical diet for juvenile northern snakehead fish (Channa argus). Anim Nutr 3:156. https://doi.org/10.1016/j.aninu.2017.03.003
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Schubert RH (1967) The taxonomy and nomenclature of the genus Aeromonas Kluyver and Van Niel 1936. Part II. Suggestions on the taxonomy and nomenclature of the anaerogenic aeromonads. Int J Syst Evol Microbiol 17:273–279. https://doi.org/10.1099/00207713-17-1-23
Suarez G, Sierra JC, Sha J, Wang S, Erova TE, Fadl AA, Foltz SM, Horneman AJ, Chopra AK (2008) Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb Pathog 44(4):344–361
Sun YL, Li XP, Sun L (2021) Pol-miR-150 regulates anti-bacterial and viral infection in Japanese flounder (Paralichthys olivaceus) via the lysosomal protein LMP2L. Comp Biochem Physiol B Biochem Mol Biol 254:110578. https://doi.org/10.1016/j.cbpb.2021.110578
Tanaka KH, Vincent AT, Trudel MV, Paquet VE, Frenette M, Charette SJ (2016) The mosaic architecture of Aeromonas salmonicida subsp. salmonicida pAsa4 plasmid and its consequences on antibiotic resistance. PeerJ 4:e2595. https://doi.org/10.7717/peerj.2595
Tanasupawat S, Ezaki T, Suzuki K, Okada S, Komagata K, Kozaki M (1992) Characterization and identification of Lactobacillus pentosus and Lactobacillus plantarum strains from fermented foods in Thailand. J Gen Appl Microbiol 38:121. https://doi.org/10.2323/jgam.38.121
Tewari R, Dudeja M, Nandy S, Das AK (2014) Isolation of Aeromonas salmonicida from human blood sample: A case report. J Clin Diagn Res 8:139. https://doi.org/10.7860/JCDR/2014/6883.4032
Vasquez I, Cao T, Hossain A, Valderrama K, Gnanagobal H, Dang M, Leeuwis R, Ness M, Campbell B, Gendron R, Kao K, Westcott J, Gamperl AK, Santander J (2020) Aeromonas salmonicida infection kinetics and protective immune response to vaccination in sablefish (Anoplopoma fimbria). Fish Shellfish Immunol 104:557. https://doi.org/10.1016/j.fsi.2020.06.005
Vincent AT, Emond-Rheault JG, Barbeau X, Attéré SA, Frenette M, Lagüe P, Charette SJ (2016) Antibiotic resistance due to an unusual ColE1-type replicon plasmid in Aeromonas salmonicida. Microbiology (Reading, Engl) 162:942. https://doi.org/10.1099/mic.0.000286
Wegleitner BJ, Tucker A, Chadderton WL, Mahon AR (2016) Identifying the genetic structure of introduced populations of northern snakehead (Channa argus) in Eastern USA. Aquat Invasions 11:199. https://doi.org/10.3391/ai.2016.11.2.09
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697. https://doi.org/10.1128/jb.173.2.697-703.1991
Whittenbury R (1963) The use of soft agar in the study of conditions affecting the utilization of fermentable substrates by lactic acid bacteria. J Gen Appl Microbiol 32:375. https://doi.org/10.1099/00221287-32-3-375
Wichardt UP, Johansson N, Ljungberg O (1989) Occurrence and distribution of Aeromonas salmonicida infections on Swedish fish farms, 1951–1987. J Aquat Anim Health 1:187. https://doi.org/10.1577/1548-8667(1989)001<0187:OADOAS>2.3.CO;2
Xu J, Bian C, Chen K, Liu G, Jiang Y, Luo Q, You X, Peng W, Li J, Huang Y, Yi Y, Dong C, Deng H, Zhang S, Zhang H, Shi Q, Xu P (2017) Draft genome of the Northern snakehead, Channa argus. GigaScience 6:1. https://doi.org/10.1093/gigascience/gix011
Yang C, Huang R, Ou M, Gui B, Zhao J, He L, Wang Y (2020) A rapid method of sex-specific marker discovery based on NGS and determination of the XX / XY sex-determination system in Channa maculata. Aquaculture 528:735499. https://doi.org/10.1016/j.aquaculture.2020.735499
Zhang DF, Xiong XL, Wang YJ, Gao YX, Ren Y, Wang Q, Shi CB (2021) Bacillus velezensis WLYS23 strain possesses antagonistic activity against hybrid snakehead bacterial pathogens. J Appl Microbiol 131:3056. https://doi.org/10.1111/jam.15162
Zhang DX, Kang YH, Song MF, Shu HP, Guo SN, Jia JP, Tao LT, Zhao ZL, Zhang L, Wang CF, Wang GQ, Qian AD, Shan XF (2019) Identity and virulence properties of Aeromonas isolates from healthy Northern snakehead (Channa argus) in China. J Appl Microbiol 69:100. https://doi.org/10.1111/lam.13172
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The work was supported by the Natural science Foundation of Shandong Province (ZR2023MC154), the National Natural Science Foundations of China (31902408, 31902402, and U1706205), the Doctoral Sustentation Fund of Qingdao Agricultural University (1120035) and the Support Plan for Youth Innovation Team of Colleges and Universities in Shandong Province (2022KJ313).
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Y.S. and P.N. contributed to study conception, literature review and writing manuscript; X.S., Q.W., Y.W., Y.T., C.Z., M.W., M.C., Z.C., X.L., Q.Z., and M.X. contributed to the execution the experiments and data analyses, manuscript writing, drawing of figures, and editing. Y.S., P.N., and S.W. supplied the chemical reagent and resources. All authors read and approved the final manuscript.
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Sun, X.N., Wang, Q., Wang, Y.F. et al. Isolation and identification of vapA-absent Aeromonas salmonicida in diseased snakehead Channa argus in China. Int Microbiol (2023). https://doi.org/10.1007/s10123-023-00455-w
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DOI: https://doi.org/10.1007/s10123-023-00455-w