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Research Paper

The Tat system and its dependent cell division proteins are critical for virulence of extra-intestinal pathogenic Escherichia coli

, , , , , , & ORCID Icon show all
Pages 1279-1292 | Received 23 Jun 2020, Accepted 28 Aug 2020, Published online: 22 Sep 2020

References

  • Tseng TT, Tyler BM, Setubal JC. Protein secretion systems in bacterial-host associations, and their description in the gene ontology. BMC Microbiol. 2009;9(Suppl 1):S2.
  • Green ER, Mecsas J. Bacterial secretion systems: an overview. Microbiol Spectr. 2016;4.
  • Bhoite S, van Gerven N, Chapman MR, et al. Curli biogenesis: bacterial amyloid assembly by the type VIII secretion pathway. EcoSal Plus. 2019;8.
  • Lauber F, Deme JC, Lea SM, et al. Type 9 secretion system structures reveal a new protein transport mechanism. Nature. 2018;564:77.
  • Palmer T, Berks BC. The twin-arginine translocation (Tat) protein export pathway. Nature Rev Microbiol. 2012;10:483–496.
  • Berks BC. The twin-arginine protein translocation pathway. Annu Rev Biochem. 2015;84:843–864.
  • Berks BC. A common export pathway for proteins binding complex redox cofactors? Mol Microbiol. 1996;22:393–404.
  • Tullman-Ercek D, DeLisa MP, Kawarasaki Y, et al. Export pathway selectivity of Escherichia coli twin arginine translocation signal peptides. J Biol Chem. 2007;282:8309–8316.
  • Berks BC, Palmer T, Sargent F. The Tat protein translocation pathway and its role in microbial physiology. Adv Microb Physiol. 2003;47:187–254.
  • Palmer T, Sargent F, Berks BC. The Tat protein export pathway. EcoSal Plus. 2010;4.
  • Ochsner UA, Snyder A, Vasil AI, et al. Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc Natl Acad Sci U S A. 2002;99:8312–8317.
  • Pradel N, Ye C, Livrelli V, et al. Contribution of the twin arginine translocation system to the virulence of enterohemorrhagic Escherichia coli O157:H7. Infect Immun. 2003;71:4908–4916.
  • Reynolds MM, Bogomolnaya L, Guo J, et al. Abrogation of the twin arginine transport system in Salmonella enterica serovar Typhimurium leads to colonization defects during infection. PloS One. 2011;6:e15800.
  • Urrutia IM, Sabag A, Valenzuela C, et al. Contribution of the twin-arginine translocation system to the intracellular survival of salmonella typhimurium in dictyostelium discoideum. Front Microbiol. 2018;9:3001.
  • Anderson MT, Mitchell LA, Zhao L, et al. Citrobacter freundii fitness during bloodstream infection. Sci Rep. 2018;8:11792.
  • Lavander M, Ericsson SK, Broms JE, et al. The twin arginine translocation system is essential for virulence of Yersinia pseudotuberculosis. Infect Immun. 2006;74:1768–1776.
  • Craig M, Sadik AY, Golubeva YA, et al. Twin-arginine translocation system (tat) mutants of Salmonella are attenuated due to envelope defects, not respiratory defects. Mol Microbiol. 2013;89:887–902.
  • Fujimoto M, Goto R, Hirota R, et al. Tat-exported peptidoglycan amidase-dependent cell division contributes to Salmonella Typhimurium fitness in the inflamed gut. PLoS Pathog. 2018;14:e1007391.
  • Bronstein PA, Marrichi M, Cartinhour S, et al. Identification of a twin-arginine translocation system in Pseudomonas syringae pv. tomato DC3000 and its contribution to pathogenicity and fitness. J Bacteriol. 2005;187:8450–8461.
  • Biran D, Ron EZ. Extraintestinal pathogenic Escherichia coli. Curr Top Microbiol Immunol. 2018;416:149–161.
  • Liu CM, Stegger M, Aziz M, et al. Escherichia coli ST131-H22 as a foodborne uropathogen. mBio. 2018;9.
  • Bergeron CR, Prussing C, Boerlin P, et al. Chicken as reservoir for extraintestinal pathogenic Escherichia coli in humans, Canada. Emerg Infect Dis. 2012;18:415–421.
  • Maluta RP, Logue CM, Casas MR, et al. Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PloS One. 2014;9:e105016.
  • Nandanwar N, Janssen T, Kuhl M, et al. Extraintestinal pathogenic Escherichia coli (ExPEC) of human and avian origin belonging to sequence type complex 95 (STC95) portray indistinguishable virulence features. Int J Med Microbiol IJMM. 2014;304:835–842.
  • Ge X Z, Jiang J, Pan Z, et al. Comparative genomic analysis shows that avian pathogenic Escherichia coli isolate IMT5155 (O2: K1:H5;ST complex 95, ST140) shares close relationship with ST95 APEC O1: k1and human ExPEC O18: k1strains. PloS One. 2014;9:e112048.
  • Gao J, Duan X, Li X, et al. Emerging of a highly pathogenic and multi-drug resistant strain of Escherichia coli causing an outbreak of colibacillosis in chickens. Infect Genet Evol. 2018;65:392–398.
  • Tan C, Xu Z, Zheng H, et al. Genome sequence of a porcine extraintestinal pathogenic Escherichia coli strain. J Bacteriol. 2011;193:5038.
  • Liu C, Zheng H, Yang M, et al. Genome analysis and in vivo virulence of porcine extraintestinal pathogenic Escherichia coli strain PCN033. BMC Genomics. 2015;16:717.
  • Tan C, Tang X, Zhang X, et al. Serotypes and virulence genes of extraintestinal pathogenic Escherichia coli isolates from diseased pigs in China. Vet J. 2012;192:483–488.
  • Zong B, Liu W, Zhang Y, et al. Effect of kpsM on the virulence of porcine extraintestinal pathogenic Escherichia coli. FEMS Microbiol Lett. 2016;363.
  • Roland K, Curtiss R 3rd, Sizemore D. Construction and evaluation of a delta cya delta crp Salmonella typhimurium strain expressing avian pathogenic Escherichia coli O78 LPS as a vaccine to prevent airsacculitis in chickens. Avian Dis. 1999;43:429–441.
  • Edwards RA, Keller LH, Schifferli DM. Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene. 1998;207:149–157.
  • Platt R, Drescher C, Park SK, et al. Genetic system for reversible integration of DNA constructs and lacZ gene fusions into the Escherichia coli chromosome. Plasmid. 2000;43:12–23.
  • Macho AP, Rufian JS, Ruiz-Albert J, et al. Competitive index: mixed infection-based virulence assays for genetic analysis in pseudomonas syringae-plant interactions. Methods Mol Biol. 2016;1363:209–217.
  • Avican U, Doruk T, Ostberg Y, et al. The Tat substrate sufi is critical for the ability of yersinia pseudotuberculosis to cause systemic infection. Infect Immun. 2017;85.
  • Hughes ER, Winter MG, Duerkop BA, et al. Microbial respiration and formate oxidation as metabolic signatures of inflammation-associated dysbiosis. Cell Host Microbe. 2017;21:208–219.
  • Zong B, Zhang Y, Wang X, et al. Characterization of multiple type-VI secretion system (T6SS) VgrG proteins in the pathogenicity and antibacterial activity of porcine extra-intestinal pathogenic Escherichia coli. Virulence. 2019;10:118–132.
  • Wang H, Liu L, Cao Q, et al. Haemophilus parasuis alpha-2,3-sialyltransferase-mediated lipooligosaccharide sialylation contributes to bacterial pathogenicity. Virulence. 2018;9:1247–1262.
  • Ize B, Stanley NR, Buchanan G, et al. Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol Microbiol. 2003;48:1183–1193.
  • Alcock F, Stansfeld PJ, Basit H, et al. Assembling the Tat protein translocase. Elife. 2016;5.
  • Bendtsen JD, Nielsen H, Widdick D, et al. Prediction of twin-arginine signal peptides. BMC Bioinformatics. 2005;6:167.
  • Cheng VW, Weiner JH. S- and N-oxide reductases. EcoSal Plus. 2007;2.
  • Cole JA, Richardson DJ. Respiration of nitrate and nitrite. EcoSal Plus. 2008;3.
  • Magalon A, Mendel RR. Biosynthesis and insertion of the molybdenum cofactor. EcoSal Plus. 2008;3.
  • Leimkuhler S, Iobbi-Nivol C. Bacterial molybdoenzymes: old enzymes for new purposes. FEMS Microbiol Rev. 2016;40:1–18.
  • Pinske C, Sawers RG. Anaerobic formate and hydrogen metabolism. EcoSal Plus. 2016;7.
  • Rivers SL, McNairn E, Blasco F, et al. Molecular genetic analysis of the moa operon of Escherichia coli K-12 required for molybdenum cofactor biosynthesis. Mol Microbiol. 1993;8:1071–1081.
  • Chaban B, Hughes HV, Beeby M. The flagellum in bacterial pathogens: for motility and a whole lot more. Semin Cell Dev Biol. 2015;46:91–103.
  • Erhardt M. Strategies to block bacterial pathogenesis by interference with motility and chemotaxis. Curr Top Microbiol Immunol. 2016;398:185–205.
  • Weller-Stuart T, Toth I, De Maayer P, et al. Swimming and twitching motility are essential for attachment and virulence of Pantoea ananatis in onion seedlings. Mol Plant Pathol. 2017;18:734–745.
  • Liu F, Fu J, Liu C, et al. Characterization and distinction of two flagellar systems in extraintestinal pathogenic Escherichia coli PCN033. Microbiol Res. 2017;196:69–79.
  • Heidrich C, Templin MF, Ursinus A, et al. Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol Microbiol. 2001;41:167–178.
  • Samaluru H, SaiSree L, Reddy M. Role of SufI (FtsP) in cell division of Escherichia coli: evidence for its involvement in stabilizing the assembly of the divisome. J Bacteriol. 2007;189:8044–8052.
  • Tarry M, Arends SJ, Roversi P, et al. The Escherichia coli cell division protein and model Tat substrate SufI (FtsP) localizes to the septal ring and has a multicopper oxidase-like structure. J Mol Biol. 2009;386:504–519.
  • Huang Q, Alcock F, Kneuper H, et al. A signal sequence suppressor mutant that stabilizes an assembled state of the twin arginine translocase. Proc Natl Acad Sci U S A. 2017;114:E1958–E67.
  • Huang Q, Palmer T. Signal peptide hydrophobicity modulates interaction with the twin-arginine translocase. mBio. 2017;8.
  • Voulhoux R, Ball G, Ize B, et al. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. Embo J. 2001;20:6735–6741.
  • Rossier O, Cianciotto NP. The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular infection. Infect Immun. 2005;73:2020–2032.
  • Xia X, Cheng L, Zhang S, et al. The role of natural antimicrobial peptides during infection and chronic inflammation. Antonie Van Leeuwenhoek. 2018;111:5–26.
  • Henderson AG, Ehre C, Button B, et al. Cystic fibrosis airway secretions exhibit mucin hyperconcentration and increased osmotic pressure. J Clin Invest. 2014;124:3047–3060.
  • Dryden M. Reactive oxygen species: a novel antimicrobial. Int J Antimicrob Agents. 2018;51:299–303.
  • Fang FC, Vazquez-Torres A. Reactive nitrogen species in host-bacterial interactions. Curr Opin Immunol. 2019;60:96–102.
  • Spratt BG. Temperature-sensitive cell division mutants of Escherichia coli with thermolabile penicillin-binding proteins. J Bacteriol. 1977;131:293–305.
  • Bernhardt TG, de Boer PA. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol Microbiol. 2003;48:1171–1182.
  • Priyadarshini R, Popham DL, Young KD. Daughter cell separation by penicillin-binding proteins and peptidoglycan amidases in Escherichia coli. J Bacteriol. 2006;188:5345–5355.
  • Grass G, Rensing C. CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem Biophys Res Commun. 2001;286:902–908.
  • Djoko KY, Chong LX, Wedd AG, et al. Reaction mechanisms of the multicopper oxidase CueO from Escherichia coli support its functional role as a cuprous oxidase. J Am Chem Soc. 2010;132:2005–2015.
  • Liochev SI, Fridovich I. The Haber-Weiss cycle – 70 years later: an alternative view. Redox Rep. 2002;7:55–57.
  • Hiniker A, Collet JF, Bardwell JC. Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC. J Biol Chem. 2005;280:33785–33791.
  • Wagner D, Maser J, Lai B, et al. Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell’s endosomal system. J Iimmunol. 2005;174:1491–1500.
  • Outten FW, Huffman DL, Hale JA, et al. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem. 2001;276:30670–30677.
  • Sheldon JR, Laakso HA, Heinrichs DE. Iron acquisition strategies of bacterial pathogens. Microbiol Spectr. 2016;4.
  • Lemos ML, Balado M. Iron uptake mechanisms as key virulence factors in bacterial fish pathogens. J Appl Microbiol. 2020;129:104–115.
  • Grosse C, Scherer J, Koch D, et al. A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli. Mol Microbiol. 2006;62:120–131.
  • Elhassanny AE, Anderson ES, Menscher EA, et al. The ferrous iron transporter FtrABCD is required for the virulence of Brucella abortus 2308 in mice. Mol Microbiol. 2013;88:1070–1082.
  • Mathew A, Eberl L, Carlier AL. A novel siderophore-independent strategy of iron uptake in the genus Burkholderia. Mol Microbiol. 2014;91:805–820.
  • Cao J, Woodhall MR, Alvarez J, et al. EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157: H7. Mol Microbiol. 2007;65:857–875.
  • Baltes N, Hennig-Pauka I, Jacobsen I, et al. Identification of dimethyl sulfoxide reductase in Actinobacillus pleuropneumoniae and its role in infection. Infect Immun. 2003;71:6784–6792.
  • Lee KM, Park Y, Bari W, et al. Activation of cholera toxin production by anaerobic respiration of trimethylamine N-oxide in Vibrio cholerae. J Biol Chem. 2012;287:39742–39752.