Cadaverine reverse transporter (CadB protein) contributes to the virulence of Aeromonas veronii TH0426

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Aeromonas veronii is one of the main pathogens causing sepsis and ulcer syndrome in freshwater fish. Analysis of the results of epidemiological investigations in recent years has revealed that the virulence of A. veronii and its tolerance to drugs have been increasing year by year. Currently, most of the research on A. veronii focuses on its isolation, identification, and drug susceptibility, whereas research on its virulence factors and pathogenesis mechanisms is relatively rare. In this study, we identified and obtained the highly expressed TH0426 cadaverine reverse transporter (CadB) of A. veronii. We used efficient suicide plasmid-mediated homologous recombination to delete the cadB gene in TH0426 and constructed a cadB deletion strain. The LD50 of ΔcadB was 93.2 times higher than that of TH0426 in zebrafish, the toxicity of ΔcadB was 9.5 times less than that of TH0426 in EPC cells, and the biofilm formation ability of ΔcadB was 5.6-fold greater than that of TH0426. In addition, motility detection results indicated that ΔcadB had lost its swimming ability. The results of flagellar staining and TEM demonstrated that ΔcadB shed the flagella. In summary, the virulence and adhesion of A. veronii TH0426 were significantly decreased by the deletion of cadB, which might provide a theoretical basis for research into A. veronii virulence factors.

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  1. Abdelhamed H, Lawrence ML, Waldbieser G (2019) Complete genome sequence data of multidrug-resistant Aeromonas veronii strain MS-18-37. Data Br 23:103689.

  2. Amal MNA, Koh CB, Nurliyana M, Suhaiba M, Nor-Amalina Z, Santha S, Diyana-Nadhirah KP, Yusof MT, Ina-Salwany MY, Zamri-Saad M (2018) A case of natural co-infection of Tilapia Lake Virus and Aeromonas veronii in a Malaysian red hybrid tilapia (Oreochromis niloticus × O. mossambicus) farm experiencing high mortality. Aquaculture 482:12–16.

  3. Auger EA, Redding KE, Plumb T, Childs LC, Meng S-Y, Bennett GN (1989) Construction of lac fusions to the inducible arginine-and lysine decarboxylase genes of Escherichia coli K12. Mol Microbiol 3(5):609–620.

  4. Chandrarathna HPSU, Nikapitiya C, Dananjaya SHS, Wijerathne CUB, Wimalasena SHMP, Kwun HJ, Heo GJ, Lee J, De Zoysa M (2018) Outcome of co-infection with opportunistic and multidrug resistant Aeromonas hydrophila and A. veronii in zebrafish: Identification, characterization, pathogenicity and immune responses. Fish Shellfish Immunol 80:573–581.

  5. Chen J, Zhu N, Kong L, Bei Y, Zheng T, Ding X, He Z (2013) First case of soft shell disease in Chinese soft-shelled turtle (Trionyx sinens) associated with Aeromonas sobria-A. veronii complex. Aquaculture 406-407:62–67.

  6. Chen PL, Tsai PJ, Chen CS, Lu YC, Chen HM, Lee NY, Lee CC, Li CW, Li MC, Wu CJ, Ko WC (2015) Aeromonas stool isolates from individuals with or without diarrhea in southern Taiwan: predominance of Aeromonas veronii. J Microbiol Immunol Infect 48(6):618–624.

  7. Dell CL, Neely MN, Olson ER (1994) Altered pH lysine signalling mutants of cadC, a gene encoding a membrane-bound transcriptional activator of the Escherichia coli cadBA operon. Mol Microbiol 14(1):7–16.

  8. Fotakis G, Timbrell JA (2006) In vitro cytotoxicity assays: comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride. Toxicol Lett 160(2):171–177.

  9. Haneburger I, Fritz G, Jurkschat N, Tetsch L, Eichinger A, Skerra A, Gerland U, Jung K (2012) Deactivation of the E. coli pH stress sensor CadC by cadaverine. J Mol Biol 424(1-2):15–27.

  10. 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(2):161–167.

  11. Igarashi K, Kashiwagi K (2019) The functional role of polyamines in eukaryotic cells. Int J Biochem Cell Biol 107:104–115.

  12. Kang GH, Lee HJ, Hwang KS, Lee S, Kim JH, Kim JS (2003) Aberrant CpG island hypermethylation of chronic gastritis, in relation to aging, gender, intestinal metaplasia, and chronic inflammation. Am J Pathol 163(4):1551–1556.

  13. 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.

  14. Khalifa AYZ, Bekhet G (2018) First isolation and characterization of the pathogenic Aeromonas veronii bv. veronii associated with ulcerative syndrome in the indigenous Pelophylax ridibundus of Al-Ahsaa, Saudi Arabia. Microb Pathog 117:361–368.

  15. Kihara H, Snell EE (2006) Spermine and related polyamines as growth stimulants for Lactobacillus casei. Proc Natl Acad Sci 43(10):867–871.

  16. Ku YH, Yu WL (2017) Extensive community-acquired pneumonia with hemophagocytic syndrome caused by Aeromonas veronii in an immunocompetent patient. J Microbiol Immunol Infect 50(4):555–556.

  17. Liu W, Tan M, Zhang C, Xu Z, Li L, Zhou R (2018) Functional characterization of murB-potABCD operon for polyamine uptake and peptidoglycan synthesis in Streptococcus suis. Microbiol Res 207:177–187.

  18. Meng SY, Bennett GN (1992) Nucleotide sequence of the Escherichia coli cad operon: a system for neutralization of low extracellular pH. J Bacteriol 174(8):2659–2669.

  19. Nawaz M, Khan SA, Khan AA, Sung K, Tran Q, Kerdahi K, Steele R (2010) Detection and characterization of virulence genes and integrons in Aeromonas veronii isolated from catfish. Food Microbiol 27(3):327–331.

  20. Neely MN, Dell CL, Olson ER (1994) Roles of LysP and CadC in mediating the lysine requirement for acid induction of the Escherichia coli cad operon. J Bacteriol 176(11):3278–3285.

  21. Patel CN, Wortham BW, Lines JL, Fetherston JD, Perry RD, Oliveira MA (2006) Polyamines are essential for the formation of plague biofilm. J Bacteriol 188(7):2355–2363.

  22. Qian J, Bu Z, Lang X, Yan G, Yang Y, Wang X, Wang X (2017) A safe and molecular-tagged Brucella canis ghosts confer protection against virulent challenge in mice. Vet Microbiol 204:121–128.

  23. Rashid MH, Kornberg A (2002) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci 97(9):4885–4890.

  24. Samie N, Noghabi KA, Gharegozloo Z, Zahiri HS, Ahmadian G, Sharafi H, Behrozi R, Vali H (2012) Psychrophilic α-amylase from Aeromonas veronii NS07 isolated from farm soils. Process Biochem 47(9):1381–1987.

  25. Schwartz EK, Heyer WD (2011) Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120(2):109–127.

  26. Shah P, Nanduri B, Swiatlo E, Ma Y, Pendarvis K (2011) Polyamine biosynthesis and transport mechanisms are crucial for fitness and pathogenesis of Streptococcus pneumoniae. Microbiology 157(Pt 2):504–515.

  27. Shiina Y, Ii K, Iwanaga M (2004) An Aeromonas veronii biovar sobria infection with disseminated intravascular gas production. J Infect Chemother 10(1):37–41.

  28. Soksawatmaekhin W, Kuraishi A, Sakata K, Kashiwagi K, Igarashi K (2004) Excretion and uptake of cadaverine by CadB and its physiological functions in Escherichia coli. Mol Microbiol 51(5):1401–1412.

  29. Song MF, Kang YH, Zhang DX, Chen L, Bi JF, Zhang HP, Zhang L, Qian AD, Shan XF (2018) Immunogenicity of extracellular products from an inactivated vaccine against Aeromonas veronii TH0426 in koi, Cyprinus carpio. Fish Shellfish Immunol 81:176–181.

  30. Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40(2):175–179.

  31. Stim-Herndon KP, Flores TM, Bennett GN (1996) Molecular characterization of adiY, a regulatory gene which affects expression of the biodegradative acid-induced arginine decarboxylase gene (adiA) of Escherichia coli. Microbiology 142(Pt 5):1311–1320.

  32. Stintzi A, Raymond KN (2000) Amonabactin-mediated iron acquisition from transferrin and lactoferrin by Aeromonas hydrophila: direct measurement of individual microscopic rate constants. J Biol Inorg Chem 5(1):57–66.

  33. Takayama M, Ohyama T, Igarashi K, Kobayashi H (1994) Escherichia coli cad operon functions as a supplier of carbon dioxide. Mol Microbiol 11(5):913–918.

  34. Vinken M, Blaauboer BJ (2017) In vitro testing of basal cytotoxicity: establishment of an adverse outcome pathway from chemical insult to cell death. Toxicol in Vitro 39:104–110.

  35. Wang J-T, Hsueh P-R, Fang C-T, Luh K-T, Chang S-C (2002) Spontaneous bacterial empyema caused by Aeromonas veronii biotype sobria. Diagn Microbiol Infect Dis 37(4):371–373.

  36. Wimalasena SHMP, De Silva BCJ, Hossain S, Pathirana HNKS, Heo GJ (2017) Prevalence and characterisation of quinolone resistance genes in Aeromonas spp. isolated from pet turtles in South Korea. J Glob Antimicrob Resist 11:34–38.

  37. Zepeda-Velázquez AP, Vega-Sánchez V, Ortega-Santana C, Rubio-Godoy M, de Oca-Mira DM, Soriano-Vargas E (2017) Pathogenicity of Mexican isolates of Aeromonas sp. in immersion experimentally-infected rainbow trout (Oncorhynchus mykiss, Walbaum 1792). Acta Trop 167:122–124.

  38. Zhou L, Wang J, Zhang LH (2007) Modulation of bacterial type III secretion system by a spermidine transporter dependent signaling pathway. PLoS One 2(12):e1291.

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Both authors made a direct intellectual contribution and approved the publication of the manuscript.

Correspondence to WuWen Sun or Xiaofeng Shan.

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All experiments were implemented in strict accordance with the Regulations of Animal Experimentation of Jilin Agricultural University (JLAU08201409), and the animal facility complied with the National Institutes of Health Guidelines for the Care and Use of Laboratory Animals (NIH Publications No. 8023).

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The authors declare that they have no competing interests.

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Tao, L., Kang, Y., Zhang, L. et al. Cadaverine reverse transporter (CadB protein) contributes to the virulence of Aeromonas veronii TH0426. Int Microbiol (2020) doi:10.1007/s10123-020-00120-6

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  • Aeromonas veronii TH0426
  • CadB
  • Virulence