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The Role of the Yersiniachelin Siderophore in the Physiology of Yersinia pestis

https://doi.org/10.21055/0370-1069-2022-4-75-81

Abstract

Pathogenic bacteria use low-molecular-weight iron chelators – siderophores – to assimilate iron in the host body. Being recognized as virulence factors, these molecules, differing in structural and functional properties, are the subject of the most intensive research in medical microbiology. The present study is devoted to the investigation of yersiniachelin siderophore (Ych) found in the causative agent of plague, Yersinia pestis. The aim of the work was to clarify the role of Ych in the physiology of Y. pestis by comparing the properties of three strains of the plague microbe, differing in Ych production. Materials and methods. Three variants of Y. pestis EV76 strain were used in the experiments: parent strain Y. pestis EV76, its mutant that does not produce Ych due to deletion of three siderophore biosynthesis genes (analogues of ypo1530–1532 in Y. pestis CO92 strain) and a complemented mutant that was transformed by a recombinant pSC-A-5EV plasmid containing Ych biosynthesis genes cloned into the high-copy plasmid vector pSC-A-amp/kan. Comparative analysis of the three strains was carried out in terms of colony morphology, siderophore activity, growth rate, and sensitivity to hydrogen peroxide. Results and discussion. The comparison of these strains has revealed that the secretion of Ych by bacteria at 26 °С ensures the assimilation of iron. At 37 °С, Ych is not secreted into the medium and protects bacteria from the bactericidal action of reactive oxygen compounds. Thus, the study shows that yersiniachelin is able to stimulate the assimilation of iron by bacteria under iron-deficit conditions and has antioxidant properties.

About the Authors

D. A. Kuznetsova
Rostov-on-Don Research Anti-Plague Institute
Russian Federation

Dar’ya A. Kuznetsova

117/40, M. Gor’kogo St., Rostov-on-Don, 344002, Russian Federation



V. A. Rykova
Rostov-on-Don Research Anti-Plague Institute
Russian Federation

117/40, M. Gor’kogo St., Rostov-on-Don, 344002, Russian Federation



O. N. Podladchikova
Rostov-on-Don Research Anti-Plague Institute
Russian Federation

117/40, M. Gor’kogo St., Rostov-on-Don, 344002, Russian Federation



References

1. Kontoghiorghes G.J., Kontoghiorghe C.N. Iron and chelation in biochemistry and medicine: new approaches to controlling iron metabolism and treating related diseases. Cells. 2020; 19(6):1456. DOI: 10.3390/cells9061456.

2. Khasheii B., Mahmoodi P., Mohammadzadeh A. Siderophores: importance in bacterial pathogenesis and applications in medicine and industry. Microbiol. Res. 2021; 250:126790. DOI: 10.1016/j.micres.2021.126790.

3. Johnstone T.C., Nolan E.M. Beyond iron: non-classical biological functions of bacterial siderophores. Dalton Trans. 2015; 44(14):6320–39. DOI: 10.1039/c4dt03559c.

4. Sia A.K., Allred B.E., Raymond K.N. Siderocalins: siderophore binding proteins evolved for primary pathogen host defense. Cur. Opin. Chem. Biol. 2013; 17(2):150–7. DOI: 10.1016/j.cbpa.2012.11.014.

5. Holden V., Bachman M.A. Diverging roles of bacterial siderophores during infection. Metallomics. 2015; 7(6):986–95. DOI: 10.1039/c4mt00333k.

6. Perry R.D., Fetherston J.D. Yersiniabactin iron uptake: mechanisms and role in Yersinia pestis pathogenesis. Microbes Infect. 2011; 13(10):808–17. DOI: 10.1016/j.micinf.2011.04.008.

7. Forman S., Paulley J.T., Fetherston J.D., Cheng Y.Q., Perry R.D. Yersinia ironomics: comparison of iron transporters among Yersinia pestis biotypes and its nearest neighbor, Yersinia pseudotuberculosis. Biometals. 2010; 23(2):275–94. DOI: 10.1007/s10534-009-9286-4.

8. Rakin A., Schneider L., Podladchikova O. Hunger for iron: the alternative siderophore iron scavenging systems in highly virulent Yersinia. Front. Cell. Inf. Microbiol. 2012; 2:151. DOI: 10.3389/fcimb.2012.00151.

9. Podladchikova O., Rykova V., Antonenka U., Rakin A. Yersinia pestis autoagglutination is mediated by Hcp-like protein and siderophore Yersiniachelin (Ych). Adv. Exp. Med. Biol. 2012; 954:289–92. DOI: 10.1007/978-1-4614-3561-7_36.

10. Kuznetsova D.A., Podladchikova O.N. [Cloning and expression of Yersinia pestis yersiniachelin siderophore biosynthesis genes in Escherichia coli cells]. Bakteriologiya [Bacteriology]. 2018; 3(1):36–44. DOI: 10.20953/2500-1027-2018-1-36-44.

11. Podladchikova O.N., Rykova V.A., Kuznetsova D.A. [Recombinant plasmid expressing cloned genes for biosynthesis of yersiniachelin siderophore of the plague pathogen, method for its production, and Y. pestis strain-superproducer of yersiniachelin]. RF Patent for an invention. 2018. No. 2670949, publ. October 25, 2018. Bull. No. 30.

12. Girard G. L’immunite dans l’infection pesteuse. Acquisitions apportees par 30 annees de travaux sur la souch de Pasteurella pestis (Girard et Robic). Biol. Med. (Paris). 1963; 52(6):631–731.

13. Podladchikova O.N., Rykova V.A., Morozova I.V. [A method for isolating an inhibitor of siderophore secretion synthesized by pgm-strains of Y. pestis and an isolated inhibitor]. RF Patent for an invention. No. 2549712, publ. April 27, 2015. Bull. No. 12.

14. Schwyn B., Neilands J.B. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 1987; 160(1):47–56. DOI: 10.1016/0003-2697(87)90612-9.

15. Motin V.L., Georgescu A.M., Fitch J.P., Gu P.P., Nelson D.O., Mabery S.L., Garnham J.B., Sokhansanj B.A., Ott L.L., Coleman M.A., Elliott J.M., Kegelmeyer L.M., Wyrobek A.J., Slezak T.R., Brubaker R.R., Garcia E. Temporal global changes in gene expression during temperature transition in Yersinia pestis. J. Bacteriol. 2004; 186(18):6298–305. DOI: 10.1128/JB.186.18.6298-6305.2004.

16. Chauvaux S., Rosso M.L., Frangeul L., Lacroix C., Labarre L., Schiavo A., Marceau M., Dillies M.A., Foulon J., Coppée J.Y., Médigue C., Simonet M., Carniel E. Transciptome analysis of Yersinia pestis in human plasma: an approach for discovering bacterial genes involved in septicaemic plague. Microbiology (Reading). 2007; 153(Pt. 9):3112–23. DOI: 10.1099/mic.0.2007/006213-0.

17. Lucier T.S., Fetherston J.D., Brubaker R.R., Perry R.D. Iron uptake and iron-repressible polypeptides in Yersinia pestis. Infect. Immun. 1996; 64(8):3023–31. DOI: 10.1128/iai.64.8.3023-3031.1996.

18. Eisendle M., Schrettl M., Kragl C., Müller D., Illmer P., Haas H. The intracellular siderophore ferricrocin is involved in iron storage, oxidative-stress resistance, germination, and sexual development in Aspergillus nidulans. Eukaryot. Cell. 2006; 5(10):1596–603. DOI: 10.1128/EC.00057-06.

19. Peralta D.R., Adler C., Corbalán N.S., Paz García E.C., Pomares M.F., Vincent P.A. Enterobactin as part of the oxidative stress response repertoire. PLoS One. 2016; 11(6):e0157799. DOI: 10.1371/journal.pone.0157799.


Review

For citations:


Kuznetsova D.A., Rykova V.A., Podladchikova O.N. The Role of the Yersiniachelin Siderophore in the Physiology of Yersinia pestis. Problems of Particularly Dangerous Infections. 2022;(4):75-81. (In Russ.) https://doi.org/10.21055/0370-1069-2022-4-75-81

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