Effect of Nutritional Determinants and TonB on the Natural Transformation of

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2021 Aug 27

PMID 34447355

Citations 4

Authors

Li Zhang

Li Huang

Mi Huang

Mengying Wang

Dekang Zhu

Mingshu Wang

Renyong Jia

Shun Chen

Xinxin Zhao

Qiao Yang

Ying Wu

Shaqiu Zhang

Juan Huang

Xumin Ou

Sai Mao

Qun Gao

Bin Tian

Anchun Cheng

Mafeng Liu

Affiliations

Soon will be listed here.

Abstract

is a gram-negative bacterium that is the first naturally competent bacterium identified in the family . However, the determinants that influence the natural transformation and the underlying mechanism remain unknown. In this study, we evaluated the effects of various nutritional factors of the GCB medium [glucose, L-glutamine, vitamin B1, Fe (NO), NaCl, phosphate, and peptone], on the natural transformation of ATCC 11845. Among the assayed nutrients, peptone and phosphate affected the natural transformation of ATCC 11845, and the transformation frequency was significantly decreased when phosphate or peptone was removed from the GCB medium. When the iron chelator 2,2'-dipyridyl (Dip) was added, the transformation frequency was decreased by approximately 100-fold and restored gradually when Fe (NO) was added, suggesting that the natural transformation of ATCC 11845 requires iron. Given the importance of TonB in nutrient transportation, we further identified whether TonB is involved in the natural transformation of ATCC 11845. Mutation of or , but not , was shown to inhibit the natural transformation of ATCC 11845 in the GCB medium. In parallel, it was shown that the mutant, but not the mutant, decreased iron acquisition in the GCB medium. This result suggested that the mutant affects the natural transformation frequency due to the deficiency of iron utilization.

Citing Articles

Basic Characterization of Natural Transformation in Avibacterium paragallinarum.

Liu D, Zhang H, Tan H, Jin Y, Zhang C, Bo Z Microbiol Spectr. 2023; 11(3):e0520922.

PMID: 37212663 PMC: 10269479. DOI: 10.1128/spectrum.05209-22.

Manganese Efflux Achieved by MetA and MetB Affects Oxidative Stress Resistance and Iron Homeostasis in Riemerella anatipestifer.

Guo F, Wang M, Huang M, Jiang Y, Gao Q, Zhu D Appl Environ Microbiol. 2023; 89(3):e0183522.

PMID: 36815770 PMC: 10057955. DOI: 10.1128/aem.01835-22.

The molecular diversity of transcriptional factor TfoX is a determinant in natural transformation in .

Tang X, Yang Z, Dai K, Liu G, Chang Y, Tang X Front Microbiol. 2022; 13:948633.

PMID: 35966685 PMC: 9372613. DOI: 10.3389/fmicb.2022.948633.

RAA Enzyme Is a New Family of Class A Extended-Spectrum β-Lactamase from Riemerella anatipestifer Strain RCAD0122.

Luo H, Zhu D, Li M, Tang Y, Zhang W, Wang H Antimicrob Agents Chemother. 2022; 66(3):e0175721.

PMID: 34978883 PMC: 8923197. DOI: 10.1128/AAC.01757-21.

References

Dubnau D, Blokesch M . Mechanisms of DNA Uptake by Naturally Competent Bacteria. Annu Rev Genet. 2019; 53:217-237. DOI: 10.1146/annurev-genet-112618-043641. View

Ganguly T, Kajfasz J, Miller J, Rabinowitz E, Galvao L, Rosalen P . Disruption of a Novel Iron Transport System Reverses Oxidative Stress Phenotypes of a Mutant Strain of Streptococcus mutans. J Bacteriol. 2018; 200(14). PMC: 6018356. DOI: 10.1128/JB.00062-18. View

Wang M, Zhang P, Zhu D, Wang M, Jia R, Chen S . Identification of the ferric iron utilization gene B739_1208 and its role in the virulence of R. anatipestifer CH-1. Vet Microbiol. 2017; 201:162-169. DOI: 10.1016/j.vetmic.2017.01.027. View

Liu M, Tian X, Wang M, Zhu D, Wang M, Jia R . Development of a markerless gene deletion strategy using rpsL as a counterselectable marker and characterization of the function of RA0C_1534 in Riemerella anatipestifer ATCC11845 using this strategy. PLoS One. 2019; 14(6):e0218241. PMC: 6557517. DOI: 10.1371/journal.pone.0218241. View

Huang L, Yuan H, Liu M, Zhao X, Wang M, Jia R . Type B Chloramphenicol Acetyltransferases Are Responsible for Chloramphenicol Resistance in , China. Front Microbiol. 2017; 8:297. PMC: 5331189. DOI: 10.3389/fmicb.2017.00297. View

Gyuris E, Wehmann E, Czeibert K, Magyar T . Antimicrobial susceptibility of Riemerella anatipestifer strains isolated from geese and ducks in Hungary. Acta Vet Hung. 2017; 65(2):153-165. DOI: 10.1556/004.2017.016. View

Hulter N, Sorum V, Borch-Pedersen K, Liljegren M, Utnes A, Primicerio R . Costs and benefits of natural transformation in Acinetobacter baylyi. BMC Microbiol. 2017; 17(1):34. PMC: 5312590. DOI: 10.1186/s12866-017-0953-2. View

Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys J . Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science. 2006; 313(5783):89-92. DOI: 10.1126/science.1127912. View

Leavitt S, Ayroud M . Riemerella anatipestifer infection of domestic ducklings. Can Vet J. 1997; 38(2):113. PMC: 1576529. View

10.

Liu M, Huang M, Zhu D, Wang M, Jia R, Chen S . Identifying the Genes Responsible for Iron-Limited Condition in CH-1 through RNA-Seq-Based Analysis. Biomed Res Int. 2017; 2017:8682057. PMC: 5429918. DOI: 10.1155/2017/8682057. View

11.

Mantilla-Calderon D, Plewa M, Michoud G, Fodelianakis S, Daffonchio D, Hong P . Water Disinfection Byproducts Increase Natural Transformation Rates of Environmental DNA in Acinetobacter baylyi ADP1. Environ Sci Technol. 2019; 53(11):6520-6528. DOI: 10.1021/acs.est.9b00692. View

12.

Frischer M, Thurmond J, Paul J . Natural plasmid transformation in a high-frequency-of-transformation marine Vibrio strain. Appl Environ Microbiol. 1990; 56(11):3439-44. PMC: 184975. DOI: 10.1128/aem.56.11.3439-3444.1990. View

13.

Karash S, Kwon Y . Iron-dependent essential genes in Salmonella Typhimurium. BMC Genomics. 2018; 19(1):610. PMC: 6092869. DOI: 10.1186/s12864-018-4986-1. View

14.

Johnsborg O, Eldholm V, Havarstein L . Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol. 2007; 158(10):767-78. DOI: 10.1016/j.resmic.2007.09.004. View

15.

Utnes A, Sorum V, Hulter N, Primicerio R, Hegstad J, Kloos J . Growth phase-specific evolutionary benefits of natural transformation in Acinetobacter baylyi. ISME J. 2015; 9(10):2221-31. PMC: 4579475. DOI: 10.1038/ismej.2015.35. View

16.

Wang X, Liu W, Zhu D, Yang L, Liu M, Yin S . Comparative genomics of Riemerella anatipestifer reveals genetic diversity. BMC Genomics. 2014; 15:479. PMC: 4103989. DOI: 10.1186/1471-2164-15-479. View

17.

Hamilton H, Dillard J . Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol. 2006; 59(2):376-85. DOI: 10.1111/j.1365-2958.2005.04964.x. View

18.

Liu M, Wang M, Zhu D, Wang M, Jia R, Chen S . Investigation of TbfA in Riemerella anatipestifer using plasmid-based methods for gene over-expression and knockdown. Sci Rep. 2016; 6:37159. PMC: 5109031. DOI: 10.1038/srep37159. View

19.

Straume D, Stamsas G, Havarstein L . Natural transformation and genome evolution in Streptococcus pneumoniae. Infect Genet Evol. 2014; 33:371-80. DOI: 10.1016/j.meegid.2014.10.020. View

20.

Liu M, Liu S, Huang M, Wang Y, Wang M, Tian X . An Exposed Outer Membrane Hemin-Binding Protein Facilitates Hemin Transport by a TonB-Dependent Receptor in Riemerella anatipestifer. Appl Environ Microbiol. 2021; 87(15):e0036721. PMC: 8276807. DOI: 10.1128/AEM.00367-21. View