Interaction of the SXT/R391 element ICE <i>Pmi</i> Jpn1 with its natural host <i>Proteus mirabilis</i>

Integrative and conjugative elements (ICEs) of the SXT/R391 family are mobile genetic elements that integrate into the bacterial host chromosome and can be transferred horizontally, spreading antimicrobial resistance genes. Our study aimed to evaluate aspects of the relationship between ICE<i>Pmi</i>Jpn1, one of the most widespread SXT/R391 variants, with its natural host <i>Proteus mirabilis</i>. For this investigation, we used isogenic strains (containing or not the ICE<i>Pmi</i>Jpn1) that enabled us to evaluate the influence of this element on several physiological aspects of <i>P. mirabilis</i> as well as the effect of different <i>P. mirabilis</i> genetic backgrounds on the conjugative transmission of the element. ICE<i>Pmi</i>Jpn1 did not impact the fitness, self-recognition, swarming, pathogenicity, and persistence abilities of this bacterium but increased biofilm formation in one strain. Additionally, conjugative transfer of the element to <i>Escherichia coli</i> is widely variable when different <i>P. mirabilis</i> strains are used as donors in mating assays. Our results indicate that ICE<i>Pmi</i>Jpn1 has no adverse effects on the physiology or pathogenicity of <i>P. mirabilis</i>, reflecting a stable association between this element and its host. Furthermore, the findings support the notion that ICE transfer between bacteria is influenced not only by element-specific regulators but also by strain-specific factors.IMPORTANCEMobile genetic elements play a key role in the spread of antimicrobial resistance, raising concerns about multidrug-resistant bacteria, yet their interactions with bacterial hosts are not well characterized. This study explores the relationship between ICE<i>Pmi</i>Jpn1, a globally distributed SXT/R391 integrative and conjugative element (ICE), and its natural host <i>Proteus mirabilis</i>, revealing minimal effects on bacterial fitness and pathogenicity. Nevertheless, strain-specific factors significantly influence conjugative transfer. These findings highlight the need for further research on host-dependent regulatory mechanisms that drive the spread of these elements. Understanding these dynamics is essential for developing strategies to mitigate the dissemination of antibiotic resistance in clinically relevant bacterial populations.

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Publication Details

Journal
Microbiology Spectrum
Published
2025-05-23
DOI
https://doi.org/10.1128/spectrum.00339-25
Citations
2
Primary Topic
Antibiotic Resistance in Bacteria
Type
article
Field-Weighted Citation Impact
1.18

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article

Interaction of the SXT/R391 element ICE Pmi Jpn1 with its natural host Proteus mirabilis

Rodrigo S. Galhardo, Kelly Ishida, Bruna Nakanishi Fortes, Douglas Lyra de Holanda Fonseca et al.
2 citations
Microbiology Spectrum
Antibiotic Resistance in Bacteria
1.18
article

Interaction of the SXT/R391 element ICE Pmi Jpn1 with its natural host Proteus mirabilis

Rodrigo S. Galhardo, Kelly Ishida, Bruna Nakanishi Fortes, Douglas Lyra de Holanda Fonseca, Gaby Scheunemann
article en
2 citations

Abstract

Integrative and conjugative elements (ICEs) of the SXT/R391 family are mobile genetic elements that integrate into the bacterial host chromosome and can be transferred horizontally, spreading antimicrobial resistance genes. Our study aimed to evaluate aspects of the relationship between ICE<i>Pmi</i>Jpn1, one of the most widespread SXT/R391 variants, with its natural host <i>Proteus mirabilis</i>. For this investigation, we used isogenic strains (containing or not the ICE<i>Pmi</i>Jpn1) that enabled us to evaluate the influence of this element on several physiological aspects of <i>P. mirabilis</i> as well as the effect of different <i>P. mirabilis</i> genetic backgrounds on the conjugative transmission of the element. ICE<i>Pmi</i>Jpn1 did not impact the fitness, self-recognition, swarming, pathogenicity, and persistence abilities of this bacterium but increased biofilm formation in one strain. Additionally, conjugative transfer of the element to <i>Escherichia coli</i> is widely variable when different <i>P. mirabilis</i> strains are used as donors in mating assays. Our results indicate that ICE<i>Pmi</i>Jpn1 has no adverse effects on the physiology or pathogenicity of <i>P. mirabilis</i>, reflecting a stable association between this element and its host. Furthermore, the findings support the notion that ICE transfer between bacteria is influenced not only by element-specific regulators but also by strain-specific factors.IMPORTANCEMobile genetic elements play a key role in the spread of antimicrobial resistance, raising concerns about multidrug-resistant bacteria, yet their interactions with bacterial hosts are not well characterized. This study explores the relationship between ICE<i>Pmi</i>Jpn1, a globally distributed SXT/R391 integrative and conjugative element (ICE), and its natural host <i>Proteus mirabilis</i>, revealing minimal effects on bacterial fitness and pathogenicity. Nevertheless, strain-specific factors significantly influence conjugative transfer. These findings highlight the need for further research on host-dependent regulatory mechanisms that drive the spread of these elements. Understanding these dynamics is essential for developing strategies to mitigate the dissemination of antibiotic resistance in clinically relevant bacterial populations.

Microbiology SpectrumVol. 13(7)
Universidade de São Paulo (BR), Institute of Biomedical Science (GB)
Fundação de Amparo à Pesquisa do Estado de São Paulo, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Openalex Percentile: Top 22%
Antibiotic Resistance in Bacteria
1.18
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