Differential Expression of Two Copies of the irmA Gene in the Enteroaggregative E. coli Strain 042

ABSTRACT Gene duplications significantly impact the gene repertoires of both eukaryotic and prokaryotic microorganisms. The genomes of pathogenic Escherichia coli strains share a group of duplicated genes whose function is mostly unknown. The irmA gene is one of the duplicates encoded in several pat...

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Main Authors: M. Bernabeu, S. Aznar, A. Prieto, M. Hüttener, A. Juárez
Format: Article
Language:English
Published: American Society for Microbiology 2022-08-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.00454-22
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author M. Bernabeu
S. Aznar
A. Prieto
M. Hüttener
A. Juárez
author_facet M. Bernabeu
S. Aznar
A. Prieto
M. Hüttener
A. Juárez
author_sort M. Bernabeu
collection DOAJ
description ABSTRACT Gene duplications significantly impact the gene repertoires of both eukaryotic and prokaryotic microorganisms. The genomes of pathogenic Escherichia coli strains share a group of duplicated genes whose function is mostly unknown. The irmA gene is one of the duplicates encoded in several pathogenic E. coli strains. The function of its gene product was investigated in the uropathogenic E. coli strain CFT073, which contains a single functional copy. The IrmA protein structure mimics that of human interleukin receptors and likely plays a role during infection. The enteroaggregative E. coli strain 042 contains two functional copies of the irmA gene. In the present work, we investigated their biological roles. The irmA_4509 allele is expressed under several growth conditions. Its expression is modulated by the global regulators OxyR and Hha, with optimal expression at 37°C and under nutritional stress conditions. Expression of the irmA_2244 allele can only be detected when the irmA_4509 allele is knocked out. Differences in the promoter regions of both alleles account for their differential expression. Our results show that under several environmental conditions, the expression of the IrmA protein in strain 042 is dictated by the irmA_4509 allele. The irmA_2244 allele appears to play a backup role to ensure IrmA expression when the irmA_4509 allele loses its function. IMPORTANCE Gene duplications occur in prokaryotic genomes at a detectable frequency. In many instances, the biological function of the duplicates is unknown, and hence, the significance of the presence of multiple copies of these genes remains unclear. In pathogenic E. coli isolates, the irmA gene can be present either as a single copy or in two or more copies. We focused our work on studying why a different pathogenic E. coli strain encodes two functional copies of the irmA gene. We show that under several environmental conditions, one of the alleles dictates IrmA expression, and the second remains silent. The latter allele is only expressed when the former is silenced. The presence of more than one functional copy of the irmA gene in some pathogenic E. coli strains can result in sufficient expression of this virulence factor during the infection process.
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spelling doaj.art-2139a45e920f4e4ab71795a3491cbe5e2022-12-22T02:13:40ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-08-0110410.1128/spectrum.00454-22Differential Expression of Two Copies of the irmA Gene in the Enteroaggregative E. coli Strain 042M. Bernabeu0S. Aznar1A. Prieto2M. Hüttener3A. Juárez4Department of Genetics, Microbiology and Statistics, Universitat de Barcelona, Barcelona, SpainInstitute for Bioengineering of Catalonia, The Barcelona Institute of Science and Technology, Barcelona, SpainDepartment of Genetics, Microbiology and Statistics, Universitat de Barcelona, Barcelona, SpainDepartment of Genetics, Microbiology and Statistics, Universitat de Barcelona, Barcelona, SpainDepartment of Genetics, Microbiology and Statistics, Universitat de Barcelona, Barcelona, SpainABSTRACT Gene duplications significantly impact the gene repertoires of both eukaryotic and prokaryotic microorganisms. The genomes of pathogenic Escherichia coli strains share a group of duplicated genes whose function is mostly unknown. The irmA gene is one of the duplicates encoded in several pathogenic E. coli strains. The function of its gene product was investigated in the uropathogenic E. coli strain CFT073, which contains a single functional copy. The IrmA protein structure mimics that of human interleukin receptors and likely plays a role during infection. The enteroaggregative E. coli strain 042 contains two functional copies of the irmA gene. In the present work, we investigated their biological roles. The irmA_4509 allele is expressed under several growth conditions. Its expression is modulated by the global regulators OxyR and Hha, with optimal expression at 37°C and under nutritional stress conditions. Expression of the irmA_2244 allele can only be detected when the irmA_4509 allele is knocked out. Differences in the promoter regions of both alleles account for their differential expression. Our results show that under several environmental conditions, the expression of the IrmA protein in strain 042 is dictated by the irmA_4509 allele. The irmA_2244 allele appears to play a backup role to ensure IrmA expression when the irmA_4509 allele loses its function. IMPORTANCE Gene duplications occur in prokaryotic genomes at a detectable frequency. In many instances, the biological function of the duplicates is unknown, and hence, the significance of the presence of multiple copies of these genes remains unclear. In pathogenic E. coli isolates, the irmA gene can be present either as a single copy or in two or more copies. We focused our work on studying why a different pathogenic E. coli strain encodes two functional copies of the irmA gene. We show that under several environmental conditions, one of the alleles dictates IrmA expression, and the second remains silent. The latter allele is only expressed when the former is silenced. The presence of more than one functional copy of the irmA gene in some pathogenic E. coli strains can result in sufficient expression of this virulence factor during the infection process.https://journals.asm.org/doi/10.1128/spectrum.00454-22enteroaggregative E. coli042gene duplicationsaec69irmA
spellingShingle M. Bernabeu
S. Aznar
A. Prieto
M. Hüttener
A. Juárez
Differential Expression of Two Copies of the irmA Gene in the Enteroaggregative E. coli Strain 042
Microbiology Spectrum
enteroaggregative E. coli
042
gene duplications
aec69
irmA
title Differential Expression of Two Copies of the irmA Gene in the Enteroaggregative E. coli Strain 042
title_full Differential Expression of Two Copies of the irmA Gene in the Enteroaggregative E. coli Strain 042
title_fullStr Differential Expression of Two Copies of the irmA Gene in the Enteroaggregative E. coli Strain 042
title_full_unstemmed Differential Expression of Two Copies of the irmA Gene in the Enteroaggregative E. coli Strain 042
title_short Differential Expression of Two Copies of the irmA Gene in the Enteroaggregative E. coli Strain 042
title_sort differential expression of two copies of the irma gene in the enteroaggregative e coli strain 042
topic enteroaggregative E. coli
042
gene duplications
aec69
irmA
url https://journals.asm.org/doi/10.1128/spectrum.00454-22
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