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Published in: European Journal of Clinical Microbiology & Infectious Diseases 11/2014

01-11-2014 | Article

The high prevalence of serine protease autotransporters of Enterobacteriaceae (SPATEs) in Escherichia coli causing neonatal septicemia

Authors: R. Tapader, S. Chatterjee, A. K. Singh, P. Dayma, S. Haldar, A. Pal, S. Basu

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 11/2014

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Abstract

Serine protease autotransporters of Enterobacteriaceae (SPATEs) are secreted proteins demonstrating diverse virulence functions. The distribution of SPATEs is studied among diarrheagenic and extraintestinal pathogenic Escherichia coli. However, the contribution of SPATEs to the virulence of neonatal septicemic Escherichia coli (NSEC) has not yet been elucidated. This study was undertaken to evaluate the prevalence and phylogenetic distribution of different subtypes of SPATEs among NSEC. The presence of virulence factors and subtypes of SPATEs among different E. coli isolates was determined by polymerase chain reaction (PCR). E. coli phylogrouping was done by triplex PCR. Clonality of the isolates was assessed by pulsed-field gel electrophoresis (PFGE). The presence of SPATEs was significantly higher among the septicemic isolates (89 %) than the fecal (7.5 %) and environmental isolates (2.5 %). Vat (vacuolating autotransporter toxin) and Sat (secreted autotransporter toxin) were found to be the two most predominant SPATEs. The incidence of SPATEs was high in septicemic isolates of phylogroups A and B1 (87 %), lacking other virulence factors. The high prevalence of SPATEs in the non-B2 phylogroups of septicemic isolates in comparison with fecal and environmental isolates indicates an association of SPATEs with NSEC. The NSEC isolates were found to be clonally distinct, suggesting that the high prevalence of SPATEs was not due to clonal relatedness of the isolates. This study is the first to show the association of SPATEs with NSEC. The presence of SPATEs in the septicemic/NSEC isolates may be considered as the most discriminatory trait studied here.
Literature
1.
go back to reference Black RE, Cousens S, Johnson HL et al (2010) Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 375:1969–1987PubMedCrossRef Black RE, Cousens S, Johnson HL et al (2010) Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 375:1969–1987PubMedCrossRef
2.
go back to reference Das P, Singh AK, Pal T, Dasgupta S, Ramamurthy T, Basu S (2011) Colonization of the gut with Gram-negative bacilli, its association with neonatal sepsis and its clinical relevance in a developing country. J Med Microbiol 60:1651–1660PubMedCrossRef Das P, Singh AK, Pal T, Dasgupta S, Ramamurthy T, Basu S (2011) Colonization of the gut with Gram-negative bacilli, its association with neonatal sepsis and its clinical relevance in a developing country. J Med Microbiol 60:1651–1660PubMedCrossRef
3.
go back to reference Zaidi AK, Thaver D, Ali SA, Khan TA (2009) Pathogens associated with sepsis in newborns and young infants in developing countries. Pediatr Infect Dis J 28:S10–S18PubMedCrossRef Zaidi AK, Thaver D, Ali SA, Khan TA (2009) Pathogens associated with sepsis in newborns and young infants in developing countries. Pediatr Infect Dis J 28:S10–S18PubMedCrossRef
4.
go back to reference Viswanathan R, Singh AK, Basu S, Chatterjee S, Sardar S, Isaacs D (2012) Multi-drug resistant gram negative bacilli causing early neonatal sepsis in India. Arch Dis Child Fetal Neonatal Ed 97:F182–F187PubMedCrossRef Viswanathan R, Singh AK, Basu S, Chatterjee S, Sardar S, Isaacs D (2012) Multi-drug resistant gram negative bacilli causing early neonatal sepsis in India. Arch Dis Child Fetal Neonatal Ed 97:F182–F187PubMedCrossRef
5.
6.
go back to reference Smith JL, Fratamico PM, Gunther NW (2007) Extraintestinal pathogenic Escherichia coli. Foodborne Pathog Dis 4:134–163PubMedCrossRef Smith JL, Fratamico PM, Gunther NW (2007) Extraintestinal pathogenic Escherichia coli. Foodborne Pathog Dis 4:134–163PubMedCrossRef
7.
go back to reference Herzer PJ, Inouye S, Inouye M, Whittam TS (1990) Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol 172:6175–6181PubMedPubMedCentral Herzer PJ, Inouye S, Inouye M, Whittam TS (1990) Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol 172:6175–6181PubMedPubMedCentral
8.
go back to reference Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558PubMedCrossRefPubMedCentral Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558PubMedCrossRefPubMedCentral
9.
go back to reference Selander RK, Korhonen TK, Väisänen-Rhen V, Williams PH, Pattison PE, Caugant DA (1986) Genetic relationships and clonal structure of strains of Escherichia coli causing neonatal septicemia and meningitis. Infect Immun 52:213–222PubMedPubMedCentral Selander RK, Korhonen TK, Väisänen-Rhen V, Williams PH, Pattison PE, Caugant DA (1986) Genetic relationships and clonal structure of strains of Escherichia coli causing neonatal septicemia and meningitis. Infect Immun 52:213–222PubMedPubMedCentral
10.
go back to reference Bingen E, Picard B, Brahimi N et al (1998) Phylogenetic analysis of Escherichia coli strains causing neonatal meningitis suggests horizontal gene transfer from a predominant pool of highly virulent B2 group strains. J Infect Dis 177:642–650PubMedCrossRef Bingen E, Picard B, Brahimi N et al (1998) Phylogenetic analysis of Escherichia coli strains causing neonatal meningitis suggests horizontal gene transfer from a predominant pool of highly virulent B2 group strains. J Infect Dis 177:642–650PubMedCrossRef
11.
go back to reference Picard B, Sevali Garcia J, Gouriou S et al (1999) The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 67:546–553PubMedPubMedCentral Picard B, Sevali Garcia J, Gouriou S et al (1999) The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 67:546–553PubMedPubMedCentral
12.
go back to reference Johnson JR, Stell AL (2000) Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 181:261–272PubMedCrossRef Johnson JR, Stell AL (2000) Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 181:261–272PubMedCrossRef
13.
go back to reference Duriez P, Clermont O, Bonacorsi S et al (2001) Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 147:1671–1676PubMed Duriez P, Clermont O, Bonacorsi S et al (2001) Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 147:1671–1676PubMed
15.
go back to reference Watt S, Lanotte P, Mereghetti L, Moulin-Schouleur M, Picard B, Quentin R (2003) Escherichia coli strains from pregnant women and neonates: intraspecies genetic distribution and prevalence of virulence factors. J Clin Microbiol 41:1929–1935PubMedCrossRefPubMedCentral Watt S, Lanotte P, Mereghetti L, Moulin-Schouleur M, Picard B, Quentin R (2003) Escherichia coli strains from pregnant women and neonates: intraspecies genetic distribution and prevalence of virulence factors. J Clin Microbiol 41:1929–1935PubMedCrossRefPubMedCentral
16.
go back to reference Ron EZ (2010) Distribution and evolution of virulence factors in septicemic Escherichia coli. Int J Med Microbiol 300:367–370PubMedCrossRef Ron EZ (2010) Distribution and evolution of virulence factors in septicemic Escherichia coli. Int J Med Microbiol 300:367–370PubMedCrossRef
17.
go back to reference Chapman TA, Wu XY, Barchia I et al (2006) Comparison of virulence gene profiles of Escherichia coli strains isolated from healthy and diarrheic swine. Appl Environ Microbiol 72:4782–4795PubMedCrossRefPubMedCentral Chapman TA, Wu XY, Barchia I et al (2006) Comparison of virulence gene profiles of Escherichia coli strains isolated from healthy and diarrheic swine. Appl Environ Microbiol 72:4782–4795PubMedCrossRefPubMedCentral
18.
go back to reference Mokady D, Gophna U, Ron EZ (2005) Virulence factors of septicemic Escherichia coli strains. Int J Med Microbiol 295:455–462PubMedCrossRef Mokady D, Gophna U, Ron EZ (2005) Virulence factors of septicemic Escherichia coli strains. Int J Med Microbiol 295:455–462PubMedCrossRef
20.
go back to reference Dautin N, Bernstein HD (2007) Protein secretion in Gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 61:89–112PubMedCrossRef Dautin N, Bernstein HD (2007) Protein secretion in Gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 61:89–112PubMedCrossRef
22.
go back to reference Yen YT, Kostakioti M, Henderson IR, Stathopoulos C (2008) Common themes and variations in serine protease autotransporters. Trends Microbiol 16:370–379PubMedCrossRef Yen YT, Kostakioti M, Henderson IR, Stathopoulos C (2008) Common themes and variations in serine protease autotransporters. Trends Microbiol 16:370–379PubMedCrossRef
23.
go back to reference Dutta PR, Cappello R, Navarro-García F, Nataro JP (2002) Functional comparison of serine protease autotransporters of Enterobacteriaceae. Infect Immun 70:7105–7113PubMedCrossRefPubMedCentral Dutta PR, Cappello R, Navarro-García F, Nataro JP (2002) Functional comparison of serine protease autotransporters of Enterobacteriaceae. Infect Immun 70:7105–7113PubMedCrossRefPubMedCentral
24.
go back to reference Boisen N, Ruiz-Perez F, Scheutz F, Krogfelt KA, Nataro JP (2009) Short report: high prevalence of serine protease autotransporter cytotoxins among strains of enteroaggregative Escherichia coli. Am J Trop Med Hyg 80:294–301PubMedPubMedCentral Boisen N, Ruiz-Perez F, Scheutz F, Krogfelt KA, Nataro JP (2009) Short report: high prevalence of serine protease autotransporter cytotoxins among strains of enteroaggregative Escherichia coli. Am J Trop Med Hyg 80:294–301PubMedPubMedCentral
25.
go back to reference Grozdanov L, Raasch C, Schulze J et al (2004) Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol 186:5432–5441PubMedCrossRefPubMedCentral Grozdanov L, Raasch C, Schulze J et al (2004) Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol 186:5432–5441PubMedCrossRefPubMedCentral
26.
go back to reference Sandt CH, Hill CW (2000) Four different genes responsible for nonimmune immunoglobulin-binding activities within a single strain of Escherichia coli. Infect Immun 68:2205–2214PubMedCrossRefPubMedCentral Sandt CH, Hill CW (2000) Four different genes responsible for nonimmune immunoglobulin-binding activities within a single strain of Escherichia coli. Infect Immun 68:2205–2214PubMedCrossRefPubMedCentral
27.
go back to reference Parham NJ, Pollard SJ, Desvaux M et al (2005) Distribution of the serine protease autotransporters of the Enterobacteriaceae among extraintestinal clinical isolates of Escherichia coli. J Clin Microbiol 43:4076–4082PubMedCrossRefPubMedCentral Parham NJ, Pollard SJ, Desvaux M et al (2005) Distribution of the serine protease autotransporters of the Enterobacteriaceae among extraintestinal clinical isolates of Escherichia coli. J Clin Microbiol 43:4076–4082PubMedCrossRefPubMedCentral
28.
go back to reference Restieri C, Garriss G, Locas MC, Dozois CM (2007) Autotransporter-encoding sequences are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Appl Environ Microbiol 73:1553–1562PubMedCrossRefPubMedCentral Restieri C, Garriss G, Locas MC, Dozois CM (2007) Autotransporter-encoding sequences are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Appl Environ Microbiol 73:1553–1562PubMedCrossRefPubMedCentral
29.
go back to reference Taddei CR, Moreno ACR, Fernandes Filho A, Montemor LPG, Martinez MB (2003) Prevalence of secreted autotransporter toxin gene among diffusely adhering Escherichia coli isolated from stools of children. FEMS Microbiol Lett 227:249–253PubMedCrossRef Taddei CR, Moreno ACR, Fernandes Filho A, Montemor LPG, Martinez MB (2003) Prevalence of secreted autotransporter toxin gene among diffusely adhering Escherichia coli isolated from stools of children. FEMS Microbiol Lett 227:249–253PubMedCrossRef
30.
go back to reference Mahjoub-Messai F, Bidet P, Caro V et al (2011) Escherichia coli isolates causing bacteremia via gut translocation and urinary tract infection in young infants exhibit different virulence genotypes. J Infect Dis 203:1844–1849PubMedCrossRef Mahjoub-Messai F, Bidet P, Caro V et al (2011) Escherichia coli isolates causing bacteremia via gut translocation and urinary tract infection in young infants exhibit different virulence genotypes. J Infect Dis 203:1844–1849PubMedCrossRef
31.
go back to reference Spurbeck RR, Dinh PC Jr, Walk ST et al (2012) Escherichia coli isolates that carry vat, fyuA, chuA, and yfcV efficiently colonize the urinary tract. Infect Immun 80:4115–4122PubMedCrossRefPubMedCentral Spurbeck RR, Dinh PC Jr, Walk ST et al (2012) Escherichia coli isolates that carry vat, fyuA, chuA, and yfcV efficiently colonize the urinary tract. Infect Immun 80:4115–4122PubMedCrossRefPubMedCentral
32.
go back to reference Roy S, Singh AK, Viswanathan R, Nandy RK, Basu S (2011) Transmission of imipenem resistance determinants during the course of an outbreak of NDM-1 Escherichia coli in a sick newborn care unit. J Antimicrob Chemother 66:2773–2780PubMedCrossRef Roy S, Singh AK, Viswanathan R, Nandy RK, Basu S (2011) Transmission of imipenem resistance determinants during the course of an outbreak of NDM-1 Escherichia coli in a sick newborn care unit. J Antimicrob Chemother 66:2773–2780PubMedCrossRef
33.
go back to reference Kuhnert P, Hacker J, Mühldorfer I, Burnens AP, Nicolet J, Frey J (1997) Detection system for Escherichia coli-specific virulence genes: absence of virulence determinants in B and C strains. Appl Environ Microbiol 63:703–709PubMedPubMedCentral Kuhnert P, Hacker J, Mühldorfer I, Burnens AP, Nicolet J, Frey J (1997) Detection system for Escherichia coli-specific virulence genes: absence of virulence determinants in B and C strains. Appl Environ Microbiol 63:703–709PubMedPubMedCentral
34.
go back to reference Yamamoto S, Terai A, Yuri K, Kurazono H, Takeda Y, Yoshida O (1995) Detection of urovirulence factors in Escherichia coli by multiplex polymerase chain reaction. FEMS Immunol Med Microbiol 12:85–90PubMedCrossRef Yamamoto S, Terai A, Yuri K, Kurazono H, Takeda Y, Yoshida O (1995) Detection of urovirulence factors in Escherichia coli by multiplex polymerase chain reaction. FEMS Immunol Med Microbiol 12:85–90PubMedCrossRef
35.
go back to reference Kotlowski R, Bernstein CN, Sepehri S, Krause DO (2007) High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 56:669–675PubMedCrossRefPubMedCentral Kotlowski R, Bernstein CN, Sepehri S, Krause DO (2007) High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 56:669–675PubMedCrossRefPubMedCentral
36.
go back to reference Abdallah KS, Cao Y, Wei DJ (2011) Epidemiologic investigation of extra-intestinal pathogenic E. coli (ExPEC) based on PCR phylogenetic group and fimH single nucleotide polymorphisms (SNPs) in China. Int J Mol Epidemiol Genet 2:339–353PubMedPubMedCentral Abdallah KS, Cao Y, Wei DJ (2011) Epidemiologic investigation of extra-intestinal pathogenic E. coli (ExPEC) based on PCR phylogenetic group and fimH single nucleotide polymorphisms (SNPs) in China. Int J Mol Epidemiol Genet 2:339–353PubMedPubMedCentral
37.
go back to reference Johnson JR, Delavari P, Kuskowski M, Stell AL (2001) Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 183:78–88PubMedCrossRef Johnson JR, Delavari P, Kuskowski M, Stell AL (2001) Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 183:78–88PubMedCrossRef
38.
go back to reference Köhler CD, Dobrindt U (2011) What defines extraintestinal pathogenic Escherichia coli? Int J Med Microbiol 301:642–647PubMedCrossRef Köhler CD, Dobrindt U (2011) What defines extraintestinal pathogenic Escherichia coli? Int J Med Microbiol 301:642–647PubMedCrossRef
Metadata
Title
The high prevalence of serine protease autotransporters of Enterobacteriaceae (SPATEs) in Escherichia coli causing neonatal septicemia
Authors
R. Tapader
S. Chatterjee
A. K. Singh
P. Dayma
S. Haldar
A. Pal
S. Basu
Publication date
01-11-2014
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 11/2014
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-014-2161-4

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