Distribution and Phylogeny of Immunoglobulin-binding Protein G in Shiga Toxin-producing Escherichia Coli and Its Association with Adherence Phenotypes

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 2010 Jun 16

PMID 20547747

Citations 10

Authors

Viktor Merkel

Barbara Ohder

Martina Bielaszewska

Wenlan Zhang

Angelika Fruth

Christian Menge

Erika Borrmann

Barbara Middendorf

Johannes Muthing

Helge Karch

Alexander Mellmann

Affiliations

Soon will be listed here.

Abstract

eibG in Shiga toxin-producing Escherichia coli (STEC) O91 encodes a protein (EibG) which binds human immunoglobulins G and A and contributes to bacterial chain-like adherence to human epithelial cells. We investigated the prevalence of eibG among STEC, the phylogeny of eibG, and eibG allelic variations and their impact on the adherence phenotype. eibG was found in 15.0% of 240 eae-negative STEC strains but in none of 157 eae-positive STEC strains. The 36 eibG-positive STEC strains belonged to 14 serotypes and to eight multilocus sequence types (STs), with serotype O91:H14/H(-) and ST33 being the most common. Sequences of the complete eibG gene (1,527 bp in size) from eibG-positive STEC resulted in 21 different alleles with 88.11% to 100% identity to the previously reported eibG sequence; they clustered into three eibG subtypes (eibG-alpha, eibG-beta, and eibG-gamma). Strains expressing EibG-alpha and EibG-beta displayed a mostly typical chain-like adherence pattern (CLAP), with formation of long chains on both human and bovine intestinal epithelial cells, whereas strains with EibG-gamma adhered in short chains, a pattern we termed atypical CLAP. The same adherence phenotypes were displayed by E. coli BL21(DE3) clones containing the respective eibG-alpha, eibG-beta, and eibG-gamma subtypes. We propose two possible evolutionary scenarios for eibG in STEC: a clonal development of eibG in strains with the same phylogenetic background or horizontal transfer of eibG between phylogenetically unrelated STEC strains.

Citing Articles

Prevalence and Implications of Shiga Toxin-Producing in Farm and Wild Ruminants.

Ray R, Singh P Pathogens. 2022; 11(11).

PMID: 36422584 PMC: 9694250. DOI: 10.3390/pathogens11111332.

Coaggregation properties of trimeric autotransporter adhesins.

Khalil H, Ogaard J, Leo J Microbiologyopen. 2020; 9(10):e1109.

PMID: 32864901 PMC: 7568254. DOI: 10.1002/mbo3.1109.

Immunogenicity of trimeric autotransporter adhesins and their potential as vaccine targets.

Thibau A, Dichter A, Vaca D, Linke D, Goldman A, Kempf V Med Microbiol Immunol. 2019; 209(3):243-263.

PMID: 31788746 PMC: 7247748. DOI: 10.1007/s00430-019-00649-y.

Molecular epidemiology of sequence type 33 of Shiga toxin-producing O91:H14 isolates from human patients and retail meats in Korea.

Lee J, Kim S, Wi S, Cho Y, Hahn T, Yu J J Vet Sci. 2018; 20(1):87-90.

PMID: 30481987 PMC: 6351770. DOI: 10.4142/jvs.2019.20.1.87.

Distinct Expression of Immunoglobulin-Binding Proteins in Shiga Toxin-Producing Escherichia coli Implicates High Protein Stability and a Characteristic Phenotype.

Rubin D, Zhang W, Karch H, Kuczius T Toxins (Basel). 2017; 9(5).

PMID: 28468281 PMC: 5450701. DOI: 10.3390/toxins9050153.

References

Mellmann A, Bielaszewska M, Zimmerhackl L, Prager R, Harmsen D, Tschape H . Enterohemorrhagic Escherichia coli in human infection: in vivo evolution of a bacterial pathogen. Clin Infect Dis. 2005; 41(6):785-92. DOI: 10.1086/432722. View

Friedrich A, Bielaszewska M, Zhang W, Pulz M, Kuczius T, Ammon A . Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis. 2002; 185(1):74-84. DOI: 10.1086/338115. View

Ochman H, Selander R . Standard reference strains of Escherichia coli from natural populations. J Bacteriol. 1984; 157(2):690-3. PMC: 215307. DOI: 10.1128/jb.157.2.690-693.1984. View

Prager R, Strutz U, Fruth A, Tschape H . Subtyping of pathogenic Escherichia coli strains using flagellar (H)-antigens: serotyping versus fliC polymorphisms. Int J Med Microbiol. 2003; 292(7-8):477-86. DOI: 10.1078/1438-4221-00226. View

Bettelheim K . The non-O157 shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit Rev Microbiol. 2007; 33(1):67-87. DOI: 10.1080/10408410601172172. View

Leveille S, Caza M, Johnson J, Clabots C, Sabri M, Dozois C . Iha from an Escherichia coli urinary tract infection outbreak clonal group A strain is expressed in vivo in the mouse urinary tract and functions as a catecholate siderophore receptor. Infect Immun. 2006; 74(6):3427-36. PMC: 1479231. DOI: 10.1128/IAI.00107-06. View

Tamura K, Dudley J, Nei M, Kumar S . MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007; 24(8):1596-9. DOI: 10.1093/molbev/msm092. View

Tarr P, Bilge S, Vary Jr J, Jelacic S, Habeeb R, Ward T . Iha: a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect Immun. 2000; 68(3):1400-7. PMC: 97294. DOI: 10.1128/IAI.68.3.1400-1407.2000. View

Bielaszewska M, Stoewe F, Fruth A, Zhang W, Prager R, Brockmeyer J . Shiga toxin, cytolethal distending toxin, and hemolysin repertoires in clinical Escherichia coli O91 isolates. J Clin Microbiol. 2009; 47(7):2061-6. PMC: 2708519. DOI: 10.1128/JCM.00201-09. View

10.

Sandt C, Hopper J, Hill C . Activation of prophage eib genes for immunoglobulin-binding proteins by genes from the IbrAB genetic island of Escherichia coli ECOR-9. J Bacteriol. 2002; 184(13):3640-8. PMC: 135156. DOI: 10.1128/JB.184.13.3640-3648.2002. View

11.

Schmidt H, Zhang W, Hemmrich U, Jelacic S, Brunder W, Tarr P . Identification and characterization of a novel genomic island integrated at selC in locus of enterocyte effacement-negative, Shiga toxin-producing Escherichia coli. Infect Immun. 2001; 69(11):6863-73. PMC: 100065. DOI: 10.1128/IAI.69.11.6863-6873.2001. View

12.

Herold S, Paton J, Paton A . Sab, a novel autotransporter of locus of enterocyte effacement-negative shiga-toxigenic Escherichia coli O113:H21, contributes to adherence and biofilm formation. Infect Immun. 2009; 77(8):3234-43. PMC: 2715694. DOI: 10.1128/IAI.00031-09. View

13.

Mellmann A, Bielaszewska M, Kock R, Friedrich A, Fruth A, Middendorf B . Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg Infect Dis. 2008; 14(8):1287-90. PMC: 2600372. DOI: 10.3201/eid1408.071082. View

14.

Smith N, Smith J, Spratt B . Sequence evolution of the porB gene of Neisseria gonorrhoeae and Neisseria meningitidis: evidence of positive Darwinian selection. Mol Biol Evol. 1995; 12(3):363-70. DOI: 10.1093/oxfordjournals.molbev.a040212. View

15.

Sandt C, HILL C . Nonimmune binding of human immunoglobulin A (IgA) and IgG Fc by distinct sequence segments of the EibF cell surface protein of Escherichia coli. Infect Immun. 2001; 69(12):7293-303. PMC: 98814. DOI: 10.1128/IAI.69.12.7293-7203.2001. View

16.

Donnenberg M, Tzipori S, McKee M, OBrien A, Alroy J, Kaper J . The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J Clin Invest. 1993; 92(3):1418-24. PMC: 288286. DOI: 10.1172/JCI116718. View

17.

Kaper J, Nataro J, Mobley H . Pathogenic Escherichia coli. Nat Rev Microbiol. 2004; 2(2):123-40. DOI: 10.1038/nrmicro818. View

18.

Werber D, Behnke S, Fruth A, Merle R, Menzler S, Glaser S . Shiga toxin-producing Escherichia coli infection in Germany: different risk factors for different age groups. Am J Epidemiol. 2006; 165(4):425-34. DOI: 10.1093/aje/kwk023. View

19.

Dugan K, Lawrence H, Hares D, Fisher C, Budowle B . An improved method for post-PCR purification for mtDNA sequence analysis. J Forensic Sci. 2002; 47(4):811-8. View

20.

Bridger P, Mohr M, Stamm I, Frohlich J, Follmann W, Birkner S . Primary bovine colonic cells: a model to study strain-specific responses to Escherichia coli. Vet Immunol Immunopathol. 2010; 137(1-2):54-63. DOI: 10.1016/j.vetimm.2010.04.010. View