Capsule-Targeting Depolymerases Derived from Prophage Regions

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2022 May 14

PMID 35563361

Authors

Alena Y Drobiazko

Anastasia A Kasimova

Peter V Evseev

Mikhail M Shneider

Evgeniy I Klimuk

Alexander S Shashkov

Andrei S Dmitrenok

Alexander O Chizhov

Pavel V Slukin

Yuriy P Skryabin

Nikolay V Volozhantsev

Konstantin A Miroshnikov

Yuriy A Knirel

Anastasia V Popova

Affiliations

Soon will be listed here.

Abstract

In this study, several different depolymerases encoded in the prophage regions of genomes have been bioinformatically predicted and recombinantly produced. The identified depolymerases possessed multi-domain structures and were identical or closely homologous to various proteins encoded in other genomes. This means that prophage-derived depolymerases are widespread, and different bacterial genomes can be the source of proteins with polysaccharide-degrading activities. For two depolymerases, the specificity to capsular polysaccharides (CPSs) of belonging to K1 and K92 capsular types (K types) was determined. The data obtained showed that the prophage-derived depolymerases were glycosidases that cleaved the CPSs by the hydrolytic mechanism to yield monomers and oligomers of the K units. The recombinant proteins with established enzymatic activity significantly reduced the mortality of larvae infected with of K1 and K92 capsular types. Therefore, these enzymes can be considered as suitable candidates for the development of new antibacterials against corresponding K types.

Citing Articles

A New Insight into Phage Combination Therapeutic Approaches Against Drug-Resistant Mixed Bacterial Infections.

Rahimian M, Jafari-Gharabaghlou D, Mohammadi E, Zarghami N Phage (New Rochelle). 2025; 5(4):203-222.

PMID: 40045937 PMC: 11876824. DOI: 10.1089/phage.2024.0011.

Antimicrobial resistance and virulence factors analysis of a multidrug-resistant Acinetobacter baumannii isolated from chickens using whole-genome sequencing.

Yu L, Zhao Y, Zhang S, Ni W, Zhang L, Xue C BMC Microbiol. 2024; 24(1):526.

PMID: 39695425 PMC: 11657679. DOI: 10.1186/s12866-024-03694-7.

Phage-encoded depolymerases as a strategy for combating multidrug-resistant .

Islam M, Mahbub N, Shin W, Oh M Front Cell Infect Microbiol. 2024; 14:1462620.

PMID: 39512587 PMC: 11540826. DOI: 10.3389/fcimb.2024.1462620.

Functional domains of bacteriophage tail fibers.

Peters D, Gaudreault F, Chen W Front Microbiol. 2024; 15:1230997.

PMID: 38690360 PMC: 11058221. DOI: 10.3389/fmicb.2024.1230997.

A novel phage putative depolymerase, Depo16, has specific activity against K1 capsular-type .

Zhao R, Jiang S, Ren S, Yang L, Han W, Guo Z Appl Environ Microbiol. 2024; 90(4):e0119723.

PMID: 38551353 PMC: 11022553. DOI: 10.1128/aem.01197-23.

References

Pires D, Oliveira H, Melo L, Sillankorva S, Azeredo J . Bacteriophage-encoded depolymerases: their diversity and biotechnological applications. Appl Microbiol Biotechnol. 2016; 100(5):2141-51. DOI: 10.1007/s00253-015-7247-0. View

Sievers F, Wilm A, Dineen D, Gibson T, Karplus K, Li W . Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011; 7:539. PMC: 3261699. DOI: 10.1038/msb.2011.75. View

Flouri T, Izquierdo-Carrasco F, Darriba D, Aberer A, Nguyen L, Minh B . The phylogenetic likelihood library. Syst Biol. 2014; 64(2):356-62. PMC: 4380035. DOI: 10.1093/sysbio/syu084. View

Loh B, Chen J, Manohar P, Yu Y, Hua X, Leptihn S . A Biological Inventory of Prophages in Genomes Reveal Distinct Distributions in Classes, Length, and Genomic Positions. Front Microbiol. 2020; 11:579802. PMC: 7744312. DOI: 10.3389/fmicb.2020.579802. View

Arndt D, Grant J, Marcu A, Sajed T, Pon A, Liang Y . PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016; 44(W1):W16-21. PMC: 4987931. DOI: 10.1093/nar/gkw387. View

Kenyon J, Kasimova A, Shneider M, Shashkov A, Arbatsky N, Popova A . The KL24 gene cluster and a genomic island encoding a Wzy polymerase contribute genes needed for synthesis of the K24 capsular polysaccharide by the multiply antibiotic resistant Acinetobacter baumannii isolate RCH51. Microbiology (Reading). 2017; 163(3):355-363. DOI: 10.1099/mic.0.000430. View

Russo T, Luke N, Beanan J, Olson R, Sauberan S, MacDonald U . The K1 capsular polysaccharide of Acinetobacter baumannii strain 307-0294 is a major virulence factor. Infect Immun. 2010; 78(9):3993-4000. PMC: 2937447. DOI: 10.1128/IAI.00366-10. View

Veerassamy S, Smith A, Tillier E . A transition probability model for amino acid substitutions from blocks. J Comput Biol. 2004; 10(6):997-1010. DOI: 10.1089/106652703322756195. View

Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J . A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 2010; 38(Web Server issue):W695-9. PMC: 2896090. DOI: 10.1093/nar/gkq313. View

10.

Popova A, Lavysh D, Klimuk E, Edelstein M, Bogun A, Shneider M . Novel Fri1-like Viruses Infecting Acinetobacter baumannii-vB_AbaP_AS11 and vB_AbaP_AS12-Characterization, Comparative Genomic Analysis, and Host-Recognition Strategy. Viruses. 2017; 9(7). PMC: 5537680. DOI: 10.3390/v9070188. View

11.

Peleg A, Seifert H, Paterson D . Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev. 2008; 21(3):538-82. PMC: 2493088. DOI: 10.1128/CMR.00058-07. View

12.

Duus J, Gotfredsen C, Bock K . Carbohydrate structural determination by NMR spectroscopy: modern methods and limitations. Chem Rev. 2001; 100(12):4589-614. DOI: 10.1021/cr990302n. View

13.

Soding J, Biegert A, Lupas A . The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005; 33(Web Server issue):W244-8. PMC: 1160169. DOI: 10.1093/nar/gki408. View

14.

Garcia-Doval C, van Raaij M . Structure of the receptor-binding carboxy-terminal domain of bacteriophage T7 tail fibers. Proc Natl Acad Sci U S A. 2012; 109(24):9390-5. PMC: 3386108. DOI: 10.1073/pnas.1119719109. View

15.

Kenyon J, Kasimova A, Sviridova A, Shpirt A, Shneider M, Mikhaylova Y . Correlation of Acinetobacter baumannii K144 and K86 capsular polysaccharide structures with genes at the K locus reveals the involvement of a novel multifunctional rhamnosyltransferase for structural synthesis. Int J Biol Macromol. 2021; 193(Pt B):1294-1300. DOI: 10.1016/j.ijbiomac.2021.10.178. View

16.

Shchurova A, Shneider M, Arbatsky N, Shashkov A, Chizhov A, Skryabin Y . Novel Myovirus TaPaz Encoding Two Tailspike Depolymerases: Characterization and Host-Recognition Strategy. Viruses. 2021; 13(6). PMC: 8228797. DOI: 10.3390/v13060978. View

17.

Singh J, Adams F, Brown M . Diversity and Function of Capsular Polysaccharide in . Front Microbiol. 2019; 9:3301. PMC: 6333632. DOI: 10.3389/fmicb.2018.03301. View

18.

McGuffin L, Aldowsari F, Alharbi S, Adiyaman R . ModFOLD8: accurate global and local quality estimates for 3D protein models. Nucleic Acids Res. 2021; 49(W1):W425-W430. PMC: 8218196. DOI: 10.1093/nar/gkab321. View

19.

Senchenkova S, Shashkov A, Popova A, Shneider M, Arbatsky N, Miroshnikov K . Structure elucidation of the capsular polysaccharide of Acinetobacter baumannii AB5075 having the KL25 capsule biosynthesis locus. Carbohydr Res. 2015; 408:8-11. DOI: 10.1016/j.carres.2015.02.011. View

20.

Liu Y, Leung S, Guo Y, Zhao L, Jiang N, Mi L . The Capsule Depolymerase Dpo48 Rescues and Mice From Systemic Infections. Front Microbiol. 2019; 10:545. PMC: 6431613. DOI: 10.3389/fmicb.2019.00545. View