دورية أكاديمية
Identification and characterization of a novel type II toxin-antitoxin system in Aeromonas veronii.
العنوان: | Identification and characterization of a novel type II toxin-antitoxin system in Aeromonas veronii. |
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المؤلفون: | Ji C; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., He T; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Wu B; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Cao X; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Fan X; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Liu X; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Li X; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Yang M; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Wang J; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Xu L; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Hu S; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Xia L; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China., Sun Y; State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, P. R. China. sunyj@hunnu.edu.cn. |
المصدر: | Archives of microbiology [Arch Microbiol] 2024 Aug 17; Vol. 206 (9), pp. 381. Date of Electronic Publication: 2024 Aug 17. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 0410427 Publication Model: Electronic Cited Medium: Internet ISSN: 1432-072X (Electronic) Linking ISSN: 03028933 NLM ISO Abbreviation: Arch Microbiol Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: Berlin, New York, Springer-Verlag. |
مواضيع طبية MeSH: | Aeromonas veronii*/genetics , Aeromonas veronii*/metabolism , Toxin-Antitoxin Systems*/genetics , Bacterial Proteins*/genetics , Bacterial Proteins*/metabolism, Bacterial Toxins/metabolism ; Bacterial Toxins/genetics ; Operon ; Escherichia coli/genetics ; Escherichia coli/metabolism ; Escherichia coli/drug effects ; Antitoxins/genetics ; Antitoxins/metabolism ; Gene Expression Regulation, Bacterial |
مستخلص: | The bacterial type II toxin-antitoxin (TA) system is a rich genetic element that participates in various physiological processes. Aeromonas veronii is the main bacterial pathogen threatening the freshwater aquaculture industry. However, the distribution of type II TA system in A. veronii was seldom documented and its roles in the life activities of A. veronii were still unexplored. In this study, a novel type II TA system AvtA-AvtT was predicted in a fish pathogen Aeromonas veronii biovar sobria with multi-drug resistance using TADB 2.0. Through an Escherichia coli host killing and rescue assay, we demonstrated that AvtA and AvtT worked as a genuine TA system, and the predicted toxin AvtT actually functioned as an antitoxin while the predicted antitoxin AvtA actually functioned as a toxin. The binding ability of AvtA with AvtT proteins were confirmed by dot blotting analysis and co-immunoprecipitation assay. Furthermore, we found that the toxin and antitoxin labelled with fluorescent proteins were co-localized. In addition, it was found that the transcription of AvtAT bicistronic operon was repressed by the AvtAT protein complex. Deletion of avtA gene and avtT gene had no obvious effect on the drug susceptibility. This study provides first characterization of type II TA system AvtA-AvtT in aquatic pathogen A. veronii. (© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.) |
References: | Catara G, Caggiano R, Palazzo L (2023) The DarT/DarG toxin-antitoxin ADP-Ribosylation system as a Novel Target for a rational design of innovative antimicrobial strategies. Pathogens 12:240. https://doi.org/10.3390/pathogens12020240. (PMID: 10.3390/pathogens12020240368395129967889) Chakraborty N, Das BK, Bera AK, Borah S, Mohanty D, Yadav AK, Kumar J, Koushlesh SK, Chanu TN, Panda SP, Vallangi R (2022) Co-prevalence of Virulence and pathogenic potential in multiple antibiotic resistant Aeromonas spp. from diseased fishes with in Silico Insight on the virulent protein network. Life-Basel 12:1979. https://doi.org/10.3390/life12121979. (PMID: 10.3390/life12121979365563449781969) Chen J, Sun R, Pan C, Sun Y, Mai B, Li QX (2020) Antibiotics and Food Safety in Aquaculture. J Agric Food Chem 68:11908–11919. https://doi.org/10.1021/acs.jafc.0c03996. (PMID: 10.1021/acs.jafc.0c0399632970417) Deter HS, Jensen RV, Mather WH, Butzin NC (2017) Mechanisms for Differential Protein production in Toxin-Antitoxin systems. Toxins 9:211. https://doi.org/10.3390/toxins9070211. (PMID: 10.3390/toxins9070211286776295535158) Dhanapala PM, Kalupahana RS, Kalupahana AW, Wijesekera DPH, Kottawatta SA, Jayasekera NK, Silva-Fletcher A, Jagoda SSSdS (2021) Characterization and Antimicrobial Resistance of Environmental and Clinical Aeromonas species isolated from Fresh Water Ornamental Fish and Associated Farming Environment in Sri Lanka. Microorganisms 9:2106. https://doi.org/10.3390/microorganisms9102106. (PMID: 10.3390/microorganisms9102106346834278537582) Fabrick JA, Tabashnik BE (2007) Binding of Bacillus thuringiensis toxin Cry1Ac to multiple sites of cadherin in pink bollworm. Insect Biochem Mol Biol 37:97–106. https://doi.org/10.1016/j.ibmb.2006.10.010. (PMID: 10.1016/j.ibmb.2006.10.01017244539) Fernandez-Bravo A, Figueras MJ (2020) An update on the Genus Aeromonas: Taxonomy, Epidemiology, and pathogenicity. Microorganisms 8:129. https://doi.org/10.3390/microorganisms8010129. (PMID: 10.3390/microorganisms8010129319634697022790) Fraikin N, Goormaghtigh F, Van Melderen L (2020) Type II toxin-antitoxin systems: Evolution and revolutions. J Bacteriol 202:e00763–e00719. https://doi.org/10.1128/jb.00763-19. (PMID: 10.1128/jb.00763-19319323117167474) Hatrongjit R, Kerdsin A, Takeuchi D, Wongsurawat T, Jenjaroenpun P, Chopjitt P, Boueroy P, Akeda Y, Hamada S (2020) Genomic Analysis of Aeromonas veronii C198, a Novel Mcr-3.41-Harboring isolate from a patient with septicemia in Thailand. Pathogens 9:1031. https://doi.org/10.3390/pathogens9121031. (PMID: 10.3390/pathogens9121031333170517763265) Hossain A, Habibullah-Al-Mamun M, Nagano I, Masunaga S, Kitazawa D, Matsuda H (2022) Antibiotics, antibiotic-resistant bacteria, and resistance genes in aquaculture: risks, current concern, and future thinking. Environ Sci Pollut Res Int 29:11054–11075. https://doi.org/10.1007/s11356-021-17825-4. (PMID: 10.1007/s11356-021-17825-435028843) Japoni-Nejad A, Mood EH, Ehsani P, Sardari S, Heravi FS, Bouzari S, Shahrokhi N (2021) Identification and characterization of the type II toxin-antitoxin systems in the carbapenem-resistant Acinetobacter baumannii. Microb Pathog 158:105052. https://doi.org/10.1016/j.micpath.2021.105052. (PMID: 10.1016/j.micpath.2021.10505234147586) Jeon H, Choi E, Hwang J (2021) Identification and characterization of VapBC toxin-antitoxin system in Bosea sp. PAMC 26642 isolated from Arctic lichens. RNA 27:1374–1389. https://doi.org/10.1261/rna.078786.121. (PMID: 10.1261/rna.078786.121344293678522696) Kato F, Yoshizumi S, Yamaguchi Y, Inouye M (2019) Genome-wide screening for identification of Novel Toxin-Antitoxin systems in Staphylococcus aureus. Appl Environ Microbiol 85:e00915. https://doi.org/10.1128/aem.00915-19. (PMID: 10.1128/aem.00915-19313754976805077) Kumar CB, Kumar A, Paria A, Kumar S, Prasad KP, Rathore G (2022) Effect of spatio-temporal variables, host fish species and on-farm biosecurity measures on the prevalence of potentially pathogenic Aeromonas species in freshwater fish farms. J Appl Microbiol 132:1700–1712. https://doi.org/10.1111/jam.15330. (PMID: 10.1111/jam.1533034664343) Lee KY, Lee BJ (2016) Structure, Biology, and therapeutic application of Toxin-Antitoxin systems in pathogenic Bacteria. Toxins 8:305. https://doi.org/10.3390/toxins8100305. (PMID: 10.3390/toxins8100305277820855086665) Li T, Raza SHA, Yang B, Sun Y, Wang G, Sun W, Qian A, Wang C, Kang Y, Shan X (2020) Aeromonas veronii infection in Commercial Freshwater Fish: a potential threat to Public Health. Animals 10:608. https://doi.org/10.3390/ani10040608. (PMID: 10.3390/ani10040608322523347222775) Ma D, Gu H, Shi Y, Huang H, Sun D, Hu Y (2021) Edwardsiella piscicida YefM-YoeB: a type II toxin-antitoxin system that is related to Antibiotic Resistance, Biofilm formation, serum survival, and Host Infection. Front Microbiol 12:646299. https://doi.org/10.3389/fmicb.2021.646299. (PMID: 10.3389/fmicb.2021.646299337322267957083) Mager A, Safran T, Engelberg-Kulka H (2021) Intracellular localization of the proteins encoded by some type II toxin-antitoxin systems in Escherichia coli. mBio 12:e01417–e01421. https://doi.org/10.1128/mBio.01417-21. (PMID: 10.1128/mBio.01417-21343405478406201) Maia JCS, Silva GAA, Cunha LSB, Gouveia GV, Goes-Neto A, Brenig B, Araujo FA, Aburjaile F, Ramos RTJ, Soares SC, Azevedo VAC, da Costa MM, Gouveia JJdS (2023) Genomic characterization of Aeromonas veronii provides insights into taxonomic assignment and reveals widespread virulence and resistance genes throughout the World. Antibiotics-Basel 12:1039. https://doi.org/10.3390/antibiotics12061039. (PMID: 10.3390/antibiotics120610393737035810295418) Ogura T, Hiraga S (1983) Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc Natl Acad Sci U S A 80:4784–4788. https://doi.org/10.1073/pnas.80.15.4784. (PMID: 10.1073/pnas.80.15.47846308648384129) Page R, Peti W (2016) Toxin-antitoxin systems in bacterial growth arrest and persistence. Nat Chem Biol 12:208–214. https://doi.org/10.1038/nchembio.2044. (PMID: 10.1038/nchembio.204426991085) Qian H, Yao Q, Tai C, Deng Z, Gan J, Ou H-Y (2018) Identification and characterization of acetyltransferase-type toxin-antitoxin locus in Klebsiella pneumoniae. Mol Microbiol 108:336–349. https://doi.org/10.1111/mmi.13934. (PMID: 10.1111/mmi.1393429461656) Qin C, Zhang Z, Wang Y, Li S, Ran C, Hu J, Xie Y, Li W, Zhou Z (2017) EPSP of L. Casei BL23 protected against the infection caused by Aeromonas veronii via Enhancement of Immune response in zebrafish. Front Microbiol 8:2406. https://doi.org/10.3389/fmicb.2017.02406. (PMID: 10.3389/fmicb.2017.02406293754855770644) Ramage HR, Connolly LE, Cox JS (2009) Comprehensive Functional Analysis of Mycobacterium tuberculosis Toxin-Antitoxin systems: implications for Pathogenesis, stress responses, and evolution. PLoS Genet 5:e1000767. https://doi.org/10.1371/journal.pgen.1000767. (PMID: 10.1371/journal.pgen.1000767200111132781298) 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. https://doi.org/10.1111/1462-2920.14390. (PMID: 10.1111/1462-2920.1439030136361) Rownicki M, Lasek R, Trylska J, Bartosik D (2020) Targeting type II toxin-antitoxin systems as antibacterial strategies. Toxins 12:568. https://doi.org/10.3390/toxins12090568. (PMID: 10.3390/toxins12090568328996347551001) Sakulworakan R, Chokmangmeepisarn P, Nguyen D-H, Sivaramasamy E, Hirono I, Chuanchuen R, Kayansamruaj P, Rodkhum C (2021) Insight into whole genome of Aeromonas veronii isolated from freshwater fish by Resistome Analysis Reveal extensively antibiotic resistant traits. Front Microbiol 12:733668. https://doi.org/10.3389/fmicb.2021.733668. (PMID: 10.3389/fmicb.2021.733668346032628484913) Sheng T, Song G, Yue T, Zhang J, Wang W, Yang Z, Lu Q (2021) Whole-genome sequencing and antimicrobial resistance analysis of multidrug-resistant Aeromonas veronii strain JC529 from a common carp. J Glob Antimicrob Resist 27:118–122. https://doi.org/10.1016/j.jgar.2021.08.007. (PMID: 10.1016/j.jgar.2021.08.00734508865) Singh A, Lankapalli AK, Mendem SK, Semmler T, Ahmed N (2024) Unraveling the evolutionary dynamics of toxin-antitoxin systems in diverse genetic lineages of Escherichia coli including the high-risk clonal complexes. mBio 15:e0302323. https://doi.org/10.1128/mbio.03023-23. (PMID: 10.1128/mbio.03023-2338117088) Song Y, Zhang S, Luo G, Shen Y, Li C, Zhu Y, Huang Q, Mou X, Tang X, Liu T, Wu S, Tong A, He Y, Bao R (2021) Type II antitoxin HigA is a Key Virulence Regulator in Pseudomonas aeruginosa. Acs Infect Dis 7:2930–2940. https://doi.org/10.1021/acsinfecdis.1c00401. (PMID: 10.1021/acsinfecdis.1c0040134554722) Sonika S, Singh S, Mishra S, Verma S (2023) Toxin-antitoxin systems in bacterial pathogenesis. Heliyon 9:e14220. https://doi.org/10.1016/j.heliyon.2023.e14220. (PMID: 10.1016/j.heliyon.2023.e142203710164310123168) 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. https://doi.org/10.1371/journal.pone.0221018. (PMID: 10.1371/journal.pone.0221018314654546715197) Williams JJ, Hergenrother PJ (2012) Artificial activation of toxin-antitoxin systems as an antibacterial strategy. Trends Microbiol 20:291–298. https://doi.org/10.1016/j.tim.2012.02.005. (PMID: 10.1016/j.tim.2012.02.005224453613952271) Xie Y, Wei Y, Shen Y, Li X, Zhou H, Tai C, Deng Z, Ou H-Y (2018) TADB 2.0: an updated database of bacterial type II toxin-antitoxin loci. Nucleic Acids Res 46:D749–D753. https://doi.org/10.1093/nar/gkx1033. (PMID: 10.1093/nar/gkx103329106666) Xu J, Xia K, Li P, Qian C, Li Y, Liang X (2020) Functional investigation of the chromosomal ccdAB and hipAB operon in Escherichia coli Nissle 1917. Appl Microbiol Biotechnol 104:6731–6747. https://doi.org/10.1007/s00253-020-10733-6. (PMID: 10.1007/s00253-020-10733-6325356957293176) Yang QE, Walsh TR (2017) Toxin-antitoxin systems and their role in disseminating and maintaining antimicrobial resistance. FEMS Microbiol Rev 41:343–353. https://doi.org/10.1093/femsre/fux006. (PMID: 10.1093/femsre/fux006284490405812544) Yao YY, Xia R, Yang YL, Hao Q, Ran C, Zhang Z, Zhou ZG (2022) Study about the combination strategy of Bacillus subtilis wt55 with AiiO-AIO6 to improve the resistance of zebrafish to Aeromonas veronii infection. Fish Shellfish Immunol 128:447–454. https://doi.org/10.1016/j.fsi.2022.08.019. (PMID: 10.1016/j.fsi.2022.08.01935985627) Yashiro Y, Sakaguchi Y, Suzuki T, Tomita K (2020) Mechanism of aminoacyl-tRNA acetylation by an aminoacyl-tRNA acetyltransferase AtaT from enterohemorrhagic E. Coli. Nat Commun 11:5438. https://doi.org/10.1038/s41467-020-19281-z. (PMID: 10.1038/s41467-020-19281-z331161457595197) Yin J, Zheng W, Gao Y, Jiang C, Shi H, Diao X, Li S, Chen H, Wang H, Li R, Li A, Xia L, Yin Y, Stewart AF, Zhang Y, Fu J (2019) Single-stranded DNA-Binding protein and exogenous RecBCD inhibitors enhance phage-derived homologous recombination in Pseudomonas. Iscience 14:1–14. https://doi.org/10.1016/j.isci.2019.03.007. (PMID: 10.1016/j.isci.2019.03.007309217326438905) Yu X, Gao X, Zhu K, Yin H, Mao X, Wojdyla JA, Qin B, Huang H, Wang M, Sun YC, Cui S (2020) Characterization of a toxin-antitoxin system in Mycobacterium tuberculosis suggests neutralization by phosphorylation as the antitoxicity mechanism. Commun Biology 3:216. https://doi.org/10.1038/s42003-020-0941-1. (PMID: 10.1038/s42003-020-0941-1) Zander I, Shmidov E, Roth S, Ben-David Y, Shoval I, Shoshani S, Danielli A, Banin E (2020) Characterization of PfiT/Pfi atoxin-antitoxin system of Pseudomonas aeruginosa that affects cell elongation and prophage induction. Environ Microbiol 22:5048–5057. https://doi.org/10.1111/1462-2920.15102. (PMID: 10.1111/1462-2920.1510232458560) Zhang S-P, Ye Y-P, Hou J, Ye Z-R, Wang Z-S, Yu X-Q, Guo D-D, Wang Y, He Y-X (2023) Antitoxin MqsA decreases antibiotic susceptibility through the global regulator AgtR in Pseudomonas fluorescens. Antimicrob Agents Chemother 67:e0081223. https://doi.org/10.1128/aac.00812-23. (PMID: 10.1128/aac.00812-2337877694) |
معلومات مُعتمدة: | 23A0053 Scientific Research Fund of Hunan Provincial Education Department; 2020JJ4055 Hunan Provincial Natural Science Foundation; XCN202137 Systematic Survey of Agricultural Microbial Germplasm Resources in Hunan Province |
فهرسة مساهمة: | Keywords: Aeromonas veronii; Antibiotic resistance; AvtA-AvtT; Type II TA system |
المشرفين على المادة: | 0 (Bacterial Proteins) 0 (Bacterial Toxins) 0 (Antitoxins) |
تواريخ الأحداث: | Date Created: 20240817 Date Completed: 20240817 Latest Revision: 20240817 |
رمز التحديث: | 20240818 |
DOI: | 10.1007/s00203-024-04101-5 |
PMID: | 39153128 |
قاعدة البيانات: | MEDLINE |
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