Molecular evolution of the pathogenicity island of enterotoxigenic Bacteroides fragilis strains

Augusto A. Franco, Rodney K. Cheng, Gyung Tae Chung, Shaoguang Wu, Hee Bok Oh, Cynthia Louise Sears

Research output: Contribution to journalArticle

Abstract

Enterotoxigenic Bacteroides fragilis (ETBF) strains, which produce a 20- kDa zinc metalloprotease toxin (BFT), have been associated with diarrheal disease in animals and young children. Studying a collection of ETBF and nontoxigenic B. fragilis (NTBF) strains, we found that bft and a second metalloprotease gene (mpII) are contained in an ~6-kb pathogenicity island (termed B. fragilis pathogenicity island or BfPAI) which is present exclusively in all 113 ETBF strains tested (pattern I). Of 191 NTBF strains, 100 (52%) lack both the BfPAI and at least a 12-kb region flanking BfPAI (pattern II), and 82 of 191 NTBF strains (43%) lack the BfPAI but contain the flanking region (pattern III). The nucleotide sequence flanking the left end of the BfPAI revealed a region with the same organization as the mobilization region of the 5-nitroimidazole resistance plasmid pIP417 and the clindamycin resistance plasmid pBFTM10, that is, two mobilization genes (bfmA and bfmB) organized in one operon and a putative origin of transfer (oriT) located in a small, compact region. The region flanking the right end of the BfPAI contains a gene (bfmC) whose predicted protein shares significant identity to the TraD mobilization proteins encoded by plasmids F and R100 from Escherichia coli, Nucleotide sequence analysis of one NTBF pattern III strain (strain I-1345) revealed that bfmB and bfmC are adjacent to each other and separated by a 16-bp GC-rich sequence. Comparison of this sequence with the appropriate sequence of ETBF strain 86-5443-2-2 showed that in this ETBF strain the 16-bp sequence is replaced by the BfPAI. This result defined the BfPAI as being 6,036 bp in length and its precise integration site as being between the bfmB and bfmC stop codons. The G+C content of the BfPAI (35%) and the flanking DNA (47 to 50%) differ greatly from that reported for the B. fragilis chromosome (42%), suggesting that the BfPAI and its flanking region are two distinct genetic elements originating from very different organisms. ETBF strains may have evolved by horizontal transfer of these two genetic elements into a pattern II NTBF strain.

Original languageEnglish (US)
Pages (from-to)6623-6633
Number of pages11
JournalJournal of Bacteriology
Volume181
Issue number21
StatePublished - Nov 1999

Fingerprint

Genomic Islands
Bacteroides fragilis
Molecular Evolution
Metalloproteases
Plasmids
GC Rich Sequence
F Factor
Genes
Animal Diseases
Clindamycin
Terminator Codon
Base Composition
Operon
Sequence Analysis
Zinc

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Immunology

Cite this

Molecular evolution of the pathogenicity island of enterotoxigenic Bacteroides fragilis strains. / Franco, Augusto A.; Cheng, Rodney K.; Chung, Gyung Tae; Wu, Shaoguang; Oh, Hee Bok; Sears, Cynthia Louise.

In: Journal of Bacteriology, Vol. 181, No. 21, 11.1999, p. 6623-6633.

Research output: Contribution to journalArticle

Franco, Augusto A. ; Cheng, Rodney K. ; Chung, Gyung Tae ; Wu, Shaoguang ; Oh, Hee Bok ; Sears, Cynthia Louise. / Molecular evolution of the pathogenicity island of enterotoxigenic Bacteroides fragilis strains. In: Journal of Bacteriology. 1999 ; Vol. 181, No. 21. pp. 6623-6633.
@article{10ffaa3ebc75437c923c7f0c10ff080b,
title = "Molecular evolution of the pathogenicity island of enterotoxigenic Bacteroides fragilis strains",
abstract = "Enterotoxigenic Bacteroides fragilis (ETBF) strains, which produce a 20- kDa zinc metalloprotease toxin (BFT), have been associated with diarrheal disease in animals and young children. Studying a collection of ETBF and nontoxigenic B. fragilis (NTBF) strains, we found that bft and a second metalloprotease gene (mpII) are contained in an ~6-kb pathogenicity island (termed B. fragilis pathogenicity island or BfPAI) which is present exclusively in all 113 ETBF strains tested (pattern I). Of 191 NTBF strains, 100 (52{\%}) lack both the BfPAI and at least a 12-kb region flanking BfPAI (pattern II), and 82 of 191 NTBF strains (43{\%}) lack the BfPAI but contain the flanking region (pattern III). The nucleotide sequence flanking the left end of the BfPAI revealed a region with the same organization as the mobilization region of the 5-nitroimidazole resistance plasmid pIP417 and the clindamycin resistance plasmid pBFTM10, that is, two mobilization genes (bfmA and bfmB) organized in one operon and a putative origin of transfer (oriT) located in a small, compact region. The region flanking the right end of the BfPAI contains a gene (bfmC) whose predicted protein shares significant identity to the TraD mobilization proteins encoded by plasmids F and R100 from Escherichia coli, Nucleotide sequence analysis of one NTBF pattern III strain (strain I-1345) revealed that bfmB and bfmC are adjacent to each other and separated by a 16-bp GC-rich sequence. Comparison of this sequence with the appropriate sequence of ETBF strain 86-5443-2-2 showed that in this ETBF strain the 16-bp sequence is replaced by the BfPAI. This result defined the BfPAI as being 6,036 bp in length and its precise integration site as being between the bfmB and bfmC stop codons. The G+C content of the BfPAI (35{\%}) and the flanking DNA (47 to 50{\%}) differ greatly from that reported for the B. fragilis chromosome (42{\%}), suggesting that the BfPAI and its flanking region are two distinct genetic elements originating from very different organisms. ETBF strains may have evolved by horizontal transfer of these two genetic elements into a pattern II NTBF strain.",
author = "Franco, {Augusto A.} and Cheng, {Rodney K.} and Chung, {Gyung Tae} and Shaoguang Wu and Oh, {Hee Bok} and Sears, {Cynthia Louise}",
year = "1999",
month = "11",
language = "English (US)",
volume = "181",
pages = "6623--6633",
journal = "Journal of Bacteriology",
issn = "0021-9193",
publisher = "American Society for Microbiology",
number = "21",

}

TY - JOUR

T1 - Molecular evolution of the pathogenicity island of enterotoxigenic Bacteroides fragilis strains

AU - Franco, Augusto A.

AU - Cheng, Rodney K.

AU - Chung, Gyung Tae

AU - Wu, Shaoguang

AU - Oh, Hee Bok

AU - Sears, Cynthia Louise

PY - 1999/11

Y1 - 1999/11

N2 - Enterotoxigenic Bacteroides fragilis (ETBF) strains, which produce a 20- kDa zinc metalloprotease toxin (BFT), have been associated with diarrheal disease in animals and young children. Studying a collection of ETBF and nontoxigenic B. fragilis (NTBF) strains, we found that bft and a second metalloprotease gene (mpII) are contained in an ~6-kb pathogenicity island (termed B. fragilis pathogenicity island or BfPAI) which is present exclusively in all 113 ETBF strains tested (pattern I). Of 191 NTBF strains, 100 (52%) lack both the BfPAI and at least a 12-kb region flanking BfPAI (pattern II), and 82 of 191 NTBF strains (43%) lack the BfPAI but contain the flanking region (pattern III). The nucleotide sequence flanking the left end of the BfPAI revealed a region with the same organization as the mobilization region of the 5-nitroimidazole resistance plasmid pIP417 and the clindamycin resistance plasmid pBFTM10, that is, two mobilization genes (bfmA and bfmB) organized in one operon and a putative origin of transfer (oriT) located in a small, compact region. The region flanking the right end of the BfPAI contains a gene (bfmC) whose predicted protein shares significant identity to the TraD mobilization proteins encoded by plasmids F and R100 from Escherichia coli, Nucleotide sequence analysis of one NTBF pattern III strain (strain I-1345) revealed that bfmB and bfmC are adjacent to each other and separated by a 16-bp GC-rich sequence. Comparison of this sequence with the appropriate sequence of ETBF strain 86-5443-2-2 showed that in this ETBF strain the 16-bp sequence is replaced by the BfPAI. This result defined the BfPAI as being 6,036 bp in length and its precise integration site as being between the bfmB and bfmC stop codons. The G+C content of the BfPAI (35%) and the flanking DNA (47 to 50%) differ greatly from that reported for the B. fragilis chromosome (42%), suggesting that the BfPAI and its flanking region are two distinct genetic elements originating from very different organisms. ETBF strains may have evolved by horizontal transfer of these two genetic elements into a pattern II NTBF strain.

AB - Enterotoxigenic Bacteroides fragilis (ETBF) strains, which produce a 20- kDa zinc metalloprotease toxin (BFT), have been associated with diarrheal disease in animals and young children. Studying a collection of ETBF and nontoxigenic B. fragilis (NTBF) strains, we found that bft and a second metalloprotease gene (mpII) are contained in an ~6-kb pathogenicity island (termed B. fragilis pathogenicity island or BfPAI) which is present exclusively in all 113 ETBF strains tested (pattern I). Of 191 NTBF strains, 100 (52%) lack both the BfPAI and at least a 12-kb region flanking BfPAI (pattern II), and 82 of 191 NTBF strains (43%) lack the BfPAI but contain the flanking region (pattern III). The nucleotide sequence flanking the left end of the BfPAI revealed a region with the same organization as the mobilization region of the 5-nitroimidazole resistance plasmid pIP417 and the clindamycin resistance plasmid pBFTM10, that is, two mobilization genes (bfmA and bfmB) organized in one operon and a putative origin of transfer (oriT) located in a small, compact region. The region flanking the right end of the BfPAI contains a gene (bfmC) whose predicted protein shares significant identity to the TraD mobilization proteins encoded by plasmids F and R100 from Escherichia coli, Nucleotide sequence analysis of one NTBF pattern III strain (strain I-1345) revealed that bfmB and bfmC are adjacent to each other and separated by a 16-bp GC-rich sequence. Comparison of this sequence with the appropriate sequence of ETBF strain 86-5443-2-2 showed that in this ETBF strain the 16-bp sequence is replaced by the BfPAI. This result defined the BfPAI as being 6,036 bp in length and its precise integration site as being between the bfmB and bfmC stop codons. The G+C content of the BfPAI (35%) and the flanking DNA (47 to 50%) differ greatly from that reported for the B. fragilis chromosome (42%), suggesting that the BfPAI and its flanking region are two distinct genetic elements originating from very different organisms. ETBF strains may have evolved by horizontal transfer of these two genetic elements into a pattern II NTBF strain.

UR - http://www.scopus.com/inward/record.url?scp=0032703884&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0032703884&partnerID=8YFLogxK

M3 - Article

C2 - 10542162

AN - SCOPUS:0032703884

VL - 181

SP - 6623

EP - 6633

JO - Journal of Bacteriology

JF - Journal of Bacteriology

SN - 0021-9193

IS - 21

ER -