Abstract
As an opportunistic pathogen, Aeromonas veronii can cause hemorrhagic septicemia of various aquatic animals. In our present study, a dominant strain SJ4, isolated from naturally infected mandarin fish (Siniperca chuatsi), was identified as A. veronii according to the morphological, physiological, and biochemical features, as well as molecular identification. Intraperitoneal injection of A. veronii SJ4 into S. chuatsi revealed clinical signs similar to the natural infection, and the median lethal dosage (LD50) of the SJ4 to S. chuatsi in a week was 3.8 × 105 CFU/mL. Histopathological analysis revealed that the isolate SJ4 could cause cell enlargement, obvious hemorrhage, and inflammatory responses in S. chuatsi. Detection of virulence genes showed the isolate SJ4 carried act, fim, flgM, ompA, lip, hly, aer, and eprCAL, and the isolate SJ4 also produce caseinase, dnase, gelatinase, and hemolysin. In addition, the complete genome of A. veronii SJ4 was sequenced, and the size of the genome of A. veronii SJ4 was 4,562,694 bp, within a G + C content of 58.95%, containing 4079 coding genes. Nine hundred ten genes encoding for several virulence factors, such as type III and VI secretion systems, flagella, motility, etc., were determined based on the VFDB database. Besides, 148 antibiotic resistance-related genes in 27 categories related to tetracyclines, fluoroquinolones, aminoglycosides, macrolides, chloramphenicol, and cephalosporins were also annotated. The present results suggested that A. veronii was etiological agent causing the bacterial septicemia of S. chuatsi in this time, as well as provided a valuable base for revealing pathogenesis and resistance mechanism of A. veronii.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Behreans A, Karber L (1953) Determination of LD50. Screening in Pharmacology. New York, NY: Academic Press
Brenner DJ, Krieg NR, Staley JT (2021) Bergey’s Manual of Systematic Bacteriology 2nd edn, vol 2, part B, Springer USA 404–406
Castro-Escarpulli G, Figueras MJ, Aguilera-Arreola G, Soler L, Fernández-Rendón E, Aparicio GO, Guarro J, Chacon MR (2003) Characterisation of Aeromonas spp. isolated from frozen fish intended for human consumption in Mexico. Int J Food Microbiol 84(1):41–49
Chen CF, Shi WZ, Zhao GZ, Li MZ (1995) Isolation and identification of pathogenic bacteria causing roted gill disease in mandarinfish Siniperca chuatsi Basilewsky. Hua Zhong Nong ye da xue xue bao= Journal Huazhong (Central China) Agricultural University 14(3):263–266
Chen N, Jiang J, Gao XJ, Li XX, Zhang Y, Liu XD, Yang H, Bing XW, Zhang XJ (2018) Histopathological analysis and the immune related gene expression profiles of mandarin fish (Siniperca chuatsi) infected with Aeromonas hydrophila. Fish Shellfish Immun 83:410–41785
De Maio N, Shaw LP, Hubbard A, George S, Sanderson ND, Swann J, Wick R, AbuOun M, Stubberfield E, Hoosdally SJ, Crook DW, Peto TEA, Sheppard AE, Bailey MJ, Read DS, Anjum MF, Walker S, Stoesser N (2019) Comparison of long-read sequencing technologies in the hybrid assembly of complex bacterial genomes. Microbiol Genomics 5:e000294
Dong H T, Techatanakitarnan C, Jindakittikul P, Thaiprayoon A, Taengphu S, Charoensapsri W, Khunrae P, Rattanarojpong T, Senapin S (2017) Aeromonas jandaei and Aeromonas veronii caused disease and mortality in Nile tilapia, Oreochromis niloticus (L.). J Fish Dis 40(10):1395–1403
Donkor ES (2013) Sequencing of bacterial genomes: principles and insights into pathogenesis and development of antibiotics. Genes 4:556–572
Fernández-Bravo A, Figueras MJ (2020) An update on the genus Aeromonas: taxonomy, epidemiology, and pathogenicity. Microorganisms 8:129
Gao X, Tong S, Zhang S, Chen Q, Jiang Z, Jiang Q, Wei W, Zhu J, Zhang X (2020) Aeromonas veronii associated with red gill disease and its induced immune response in Macrobrachium nipponense. Aquac Res 51:5163–5174
González-Serrano CJ, Santos JA, García-López ML, Otero A (2002) Virulence markers in Aeromonas hydrophila and Aeromonas veronii biovar sobria isolates from freshwater fish and from a diarrhoea case. J Appl Microbiol 93:414–419
Haslinger-Löffler B, Kahl BC, Grundmeier M, Strangfeld K, Wagner B, Fischer U, Cheung AL, Peters G, Schulze OK, Sinha B (2005) Multiple virulence factors are required for Staphylococcus aureus-induced apoptosis in endothelial cells. Cell Microbiol 7:1087–1097
Hassan MA, Noureldin EA, Mahmoud MA, Fita NA (2017) Molecular identification and epizootiology of Aeromonas veronii infection among farmed Oreochromis niloticus in Eastern Province, KSA. Egypt J Aquat Res 43:161–167
Huang X, Wu C, Deng Y, Wang K, Geng Y, Zhao J (2010) Pathohistological observation of Ictalurus punctatus infected with Aeromonas veronii. Chinese Veterinary Science/zhongguo Shouyi Kexue 40:738–742
Janda JM, Abbott SL (2010) The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 23:35–73
Kang Y, Pan X, Xu Y, Siddiqui SA, Wang C, Shan X, Qian A (2016) Complete genome sequence of the fish pathogen Aeromonas veronii TH0426 with potential application in biosynthesis of pullulanase and chitinase. J Biotechnol 227:81–82
Kaur A, Holeyappa SA, Bansal N, Kaur VI, Tyagi A (2020) Ameliorative effect of turmeric supplementation in feed of Labeo rohita (Linn.) challenged with pathogenic Aeromonas veronii. Aquacult Int 28:1169–1182
Kim JD, Do JW, Choi HS, Seo JS, Jung SH, Jo HI, Park MA, Lee NS, Park SW (2013) Pathological changes in cultured Korean catfish (Silurus asotus) artficially infected with Aeromonas veronii. Korean J Environ Biol 31:486–492
Kingombe CIB, Huys G, Tonolla M, Albert MJ, Swings J, Peduzzi R, Jemmi T (1999) PCR detection, characterization, and distribution of virulence genes in Aeromonas spp. Appl Environ Microb 65:5293–5302
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874
Lin Q, Li J, Fu X, Liu L, Liang H, Niu Y, Huang C, Huang Z, Mo Z, Li N (2020) Hemorrhagic gill disease of Chinese perch caused by Aeromonas salmonicida subsp. salmonicida in China. Aquaculture 519:734775
Liu F, Yuwono C, Tay ACY, Wehrhahn MC, Riordan SM, Zhang L (2022a) Analysis of global Aeromonas veronii genomes provides novel information on source of infection and virulence in human gastrointestinal diseases. BMC Genomics 23:1–15
Liu G, Li J, Jiang Z, Zhu X, Gao X, Jiang Q, Wang J, Wei W, Zhang X (2022b) Pathogenicity of Aeromonas veronii causing mass mortalities of Odontobutis potamophila and its induced host immune response. Fish Shellfish Immun 125:180–189
Luo X, Fu X, Liao G, Chang O, Huang Z, Li N (2017) Isolation, pathogenicity and characterization of a novel bacterial pathogen Streptococcus uberis from diseased mandarin fish Siniperca chuatsi. Microb Pathogenesis 107:380–389
Martínez JL, Baquero F (2002) Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance. Clin Microbiol Rev 15:647–679
Matys J, Turska-Szewczuk A, Sroka-Bartnicka A (2020) Role of bacterial secretion systems and effector proteins–insights into Aeromonas pathogenicity mechanisms. Acta Biochim Pol 67:283–293
Miller WR, Munita JM, Arias CA (2014) Mechanisms of antibiotic resistance in enterococci. Expert Rev Anti-Infe 12:1221–1236
Mishra SS, Rakesh D, Dhiman M, Choudhary P, Debbarma J, Sahoo SN, Mishra CK (2017) Present status of fish disease management in freshwater aquaculture in India: state-of-the-art-review. Journal of Aquaculture & Fisheries 1:14
Nailis H, Kucharíková S, Řičicová M, Van Dijck P, Deforce D, Nelis H, Coenye T (2010) Real-time PCR expression profiling of genes encoding potential virulence factors in Candida albicans biofilms: identification of model-dependent and-independent gene expression. BMC Microbiol 10:1–11
Pang M, Jiang J, Xie X, Wu Y, Dong Y, Kwok AH, Zhang W, Yao H, Lu C, Leung FC, Liu Y (2015) Novel insights into the pathogenicity of epidemic Aeromonas hydrophila ST251 clones from comparative genomics. Sci Rep-UK 5:9833
Pei C, Song H, Zhu L, Qiao D, Yan Y, Li L, Zhao XL, Zhang J, Jiang XY, Kong X (2021) Identification of Aeromonas veronii isolated from largemouth bass Micropterus salmoides and histopathological analysis. Aquaculture 540:736707
Ran C, Qin C, Xie M, Zhang J, Li J, Xie Y, Wang Y, Li S, Liu L, Fu X, Lin Q, Li N, Liles MR, Zhou Z (2018) Aeromonas veronii and aerolysin are important for the pathogenesis of motile aeromonad septicemia in cyprinid fish. Environ Microbiol 20:3442–3456
Shameena SS, Kumar K, Kumar S, Kumar S, Rathore G (2020) Virulence characteristics of Aeromonas veronii biovars isolated from infected freshwater goldfish (Carassius auratus). Aquaculture 518:734819
Sharma AK, Dhasmana N, Dubey N, Kumar N, Gangwal A, Gupta M, Singh Y (2017) Bacterial virulence factors: secreted for survival. Indian J Microbiol 57:1–10
Shen Y, Wu Y, Wang Y, Li L, Li C, Zhao Y, Yang S (2021) Contribution of autochthonous microbiota succession to flavor formation during Chinese fermented mandarin fish (Siniperca chuatsi). Food Chem 348:129107
Smyrli M, Prapas A, Rigos G, Kokkari C, Pavlidis M, Katharios P (2017) Aeromonas veronii infection associated with high morbidity and mortality in farmed European seabass Dicentrarchus labrax in the Aegean Sea. Greece Fish Pathol 52:68–81
Sreedharan K, Philip R, Singh IB (2011) Isolation and characterization of virulent Aeromonas veronii from ascitic fluid of oscar Astronotus ocellatus showing signs of infectious dropsy. Dis Aquat Organ 94:29–39
Sughra F, Hafeez-ur-Rehman M, Abbas F, Altaf I, Hassan Z, Bhatti A, Ali K (2022) Molecular characterisation and genetic analysis of aerolysin and haemolysin in Aeromonas hydrophila isolated from diseased Labeo rohita by polymerase chain reaction. J Fish 10:103402–103402
Sun JJ, Zhang XJ, Gao XJ, Jiang Q, Wen Y, Lin L (2016) Characterization of virulence properties of Aeromonas veronii isolated from diseased Gibel Carp (Carassius gibelio). Int J Mol Sci 17:496.
Tekedar HC, Kumru S, Blom J, Perkins AD, Griffin MJ, Abdelhamed H, Karsi A, Lawrence ML (2019) Comparative genomics of Aeromonas veronii: identification of a pathotype impacting aquaculture globally. PLoS ONE 14:e0221018
Tyagi A, Sharma C, Srivastava A, Kumar BN, Pathak D, Rai S (2022) Isolation, characterization and complete genome sequencing of fish pathogenic Aeromonas veronii from diseased Labeo rohita. Aquaculture 553:738085
Wang B, Mao C, Feng J, Li Y, Hu J, Jiang B, Gu Q, Su Y (2021) A first report of Aeromonas veronii infection of the sea bass, Lateolabrax maculatus in China. Front Vet Sci 7:600587
Wang P, Wen Z, Li B, Zeng Z, Wang X (2016) Complete genome sequence of Vibrio alginolyticus ATCC 33787T isolated from seawater with three native megaplasmids. Mar Genom 28:45–47
Zeb S, Shah MA, Yasir M, Awan HM, Prommeenate P, Klanchui A, Wren BW, Thomson N, Bokhari H (2019) Type III secretion system confers enhanced virulence in clinical non-O1/non-O139 Vibrio cholerae. Microb Pathogenesis 135:103645
Zhang HP, Chen MY, Xu YX, Xu GY, Chen JR, Wang YM, Kang YH, Shan XF, Kong LC, Ma HX (2020) An effective live attenuated vaccine against Aeromonas veronii infection in the loach (Misgurnus anguillicaudatus). Fish Shellfish Immun 104:269–278
Zhang XJ, Bai XS, Yan BL, Bi KR, Qin L (2014) Vibrio harveyi as a causative agent of mass mortalities of megalopa in the seed production of swimming crab Portunus trituberculatus. Aquacult Int 22:661–672
Zhou W, Zhang Y, Wen Y, Ji W, Zhou Y, Ji Y, Liu X, Wang W, Asim M, Liang X, Ai T, Lin L (2015) Analysis of the transcriptomic profilings of Mandarin fish (Siniperca chuatsi) infected with Flavobacterium columnare with an emphasis on immune responses. Fish Shellfish Immun 43:111–119
Zhou Y, Gu S, Li J, Ji P, Zhang Y, Wu C, Jiang Q, Gao X, Zhang X (2022) Complete genome analysis of highly pathogenic non-O1/O139 Vibrio cholerae isolated from Macrobrachium rosenbergii reveals pathogenicity and antibiotic resistance-related genes. Front Vet Sci 9:882–885
Zhu X, Qian Q, Wu C, Zhu Y, Gao X, Jiang Q, Wang J, Liu G, Zhang X (2022) Pathogenicity of Aeromonas veronii causing mass mortality of largemouth bass (Micropterus salmoides) and its induced host immune response. Microorganisms 10:2198
Funding
This work was supported by the “JBGS” Project of Seed Industry Revitalization in Jiangsu Province (JBGS (2021) 132).
Author information
Authors and Affiliations
Contributions
X.H. Zhu finished writing—original draft, methodology, conceptualization, and data curation. L.J. Qin finished methodology and data curation. Q.Q. Qian finished methodology, data curation. Y.J. Zhu finished methodology, data curation. X.J. Gao finished writing—review. Qun Jiang finished methodology. Jun Wang finished data curation. Guoxing Liu supported funding acquisition. Xiaojun Zhang finished the writing—review, conceptualization and funding acquisition. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Ethics Approval
All treatments involving animals were carried out under the strict guidelines of Animal Experiment Ethics Committee of Yangzhou University. (Permit number: 201802003).
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhu, X., Qin, L., Zhu, Y. et al. Characteristics and Complete Genome Analysis of a Pathogenic Aeromonas Veronii SJ4 from Diseased Siniperca Chuatsi. Mar Biotechnol 25, 966–982 (2023). https://doi.org/10.1007/s10126-023-10253-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-023-10253-0