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Mobile genetic elements-driven partitions of mega-plasmids resistome in Salmonella Infantis.

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Τίτλος: Mobile genetic elements-driven partitions of mega-plasmids resistome in Salmonella Infantis.
Συγγραφείς: Zhang Y; Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, California, USA., Chu M; Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, California, USA., Liao Y-T; Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, California, USA., Wu VCH; Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, California, USA.
Πηγή: Microbiology spectrum [Microbiol Spectr] 2026 Sep; Vol. 14 (9), pp. e0182725. Date of Electronic Publication: 2026 Jul 23.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: ASM Press Country of Publication: United States NLM ID: 101634614 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2165-0497 (Electronic) Linking ISSN: 21650497 NLM ISO Abbreviation: Microbiol Spectr Subsets: MEDLINE
Imprint Name(s): Original Publication: Washington, DC : ASM Press, 2013-
Ιατρικοί όροι (MeSH): Salmonella enterica*/genetics , Salmonella enterica*/drug effects , Plasmids*/genetics , Interspersed Repetitive Sequences*, Virulence Factors/genetics ; Anti-Bacterial Agents/pharmacology ; Salmonella Infections/microbiology ; Drug Resistance, Bacterial/genetics ; Salmonella/genetics ; Drug Resistance, Multiple, Bacterial/genetics ; Gene Transfer, Horizontal ; Humans ; Genome, Bacterial
Περίληψη: Salmonella enterica serovar Infantis (S. Infantis) becomes the primary pathogen among the top Salmonella serotypes, contributing to numerous cases of foodborne illness annually in the United States. S. Infantis infection has spread rapidly worldwide, especially the clones with pESI-like plasmids. However, the underlying mechanisms regarding the transmission of S. Infantis, particularly mobile genetic elements (MGEs), mediated horizontal gene transfer, are limited. The objective of this study was to evaluate the relationship, if any, among MGEs, antibiotic-resistant genes (ARGs), and virulence factors (VFs) within S. Infantis via genomic analysis. A total of 91 S. Infantis complete genomes with high sequencing quality were selected for downstream bioinformatic analysis. The results showed that the majority of VFs were located in the bacterial chromosomes, while most ARGs were carried by S. Infantis mega-plasmids in an MGE-favored manner. Integrons and transposons were closely associated with certain ARGs, but prophages within mega-plasmids displayed a diverse ARG profile. Collectively, MGE-mediated horizontal gene transfer might lead to ARG acquisition by mega-plasmids, subsequently contributing to the resistome of S. Infantis. Our findings provide insights into the development of MGE-associated resistome in S. Infantis that could inform more effective prevention and intervention strategies to control this pathogen, further ensuring public health and safety.IMPORTANCEThe rapid emergence and transmission of antibiotic-resistant foodborne pathogens pose a significant risk to public health, necessitating the discovery of underlying mechanisms to control multidrug-resistant pathogens. Salmonella enterica serovar Infantis (S. Infantis) has become a pathogen of clinical and epidemiological relevance in recent years, ranking as the top prevalent serovar associated with foodborne illnesses and exhibiting resistance to several antibiotics. The current investigation of multidrug resistance (MDR) S. Infantis strains primarily emphasized the presence of mega-plasmids. However, the question of how mega-plasmids contribute to the transmission of antibiotic-resistant genes (ARG) is unaddressed. Utilizing the genomic characterization of S. Infantis complete genomes with high quality, our study revealed that the resistome of S. Infantis mega-plasmids-the primary ARG reservoirs of S. Infantis-followed a specific pattern of mobile genetic elements (MGEs). Monitoring the spread of MGE-carried ARGs within mega-plasmids should be considered in future surveillance.
Competing Interests: The authors declare no conflict of interest.
References: Emerg Infect Dis. 2023 Aug;29(8):1634-1637. (PMID: 37486207)
Microb Genom. 2022 Jan;8(1):. (PMID: 35072601)
Environ Microbiol. 2014 Apr;16(4):977-94. (PMID: 24320043)
EFSA J. 2021 Apr 12;19(4):e06490. (PMID: 33868492)
BMC Genomics. 2019 Nov 15;20(1):870. (PMID: 31730461)
mSystems. 2016 Jun 21;1(3):. (PMID: 27822532)
Front Microbiol. 2021 Jul 23;12:649969. (PMID: 34367079)
BMC Genom Data. 2025 Feb 28;26(1):15. (PMID: 40022005)
Mol Biol Evol. 2021 Sep 27;38(10):4647-4654. (PMID: 34320186)
Int J Food Microbiol. 2020 Apr 16;319:108497. (PMID: 31927155)
Nucleic Acids Res. 2024 Jul 5;52(W1):W78-W82. (PMID: 38613393)
Nucleic Acids Res. 2016 Jul 8;44(W1):W16-21. (PMID: 27141966)
Mol Biol Evol. 2009 Jul;26(7):1641-50. (PMID: 19377059)
Front Microbiol. 2018 May 04;9:836. (PMID: 29780368)
J Clin Microbiol. 2015 May;53(5):1685-92. (PMID: 25762776)
Microorganisms. 2023 Feb 21;11(3):. (PMID: 36985115)
Antimicrob Agents Chemother. 2017 Jun 27;61(7):. (PMID: 28483962)
Poult Sci. 2024 Apr;103(4):103516. (PMID: 38368739)
PLoS One. 2024 Mar 14;19(3):e0299354. (PMID: 38483966)
Nucleic Acids Res. 2025 Jan 6;53(D1):D871-D877. (PMID: 39470738)
Prev Vet Med. 2025 Jan;234:106364. (PMID: 39510009)
Mol Microbiol. 2019 Feb;111(2):303-316. (PMID: 30466179)
Bioessays. 2017 Dec;39(12):. (PMID: 28983932)
Front Microbiol. 2020 Jan 21;10:3093. (PMID: 32038541)
Int J Food Microbiol. 2025 Mar 16;432:111090. (PMID: 39919607)
Curr Opin Microbiol. 2005 Aug;8(4):451-8. (PMID: 16019256)
Brief Funct Genomics. 2013 Jul;12(4):354-65. (PMID: 23520178)
Antimicrob Agents Chemother. 2014 Jul;58(7):3895-903. (PMID: 24777092)
Microorganisms. 2022 Jul 21;10(7):. (PMID: 35889197)
Microbiol Spectr. 2024 May 2;12(5):e0004724. (PMID: 38546218)
Microbiol Spectr. 2022 Dec 21;10(6):e0248122. (PMID: 36250854)
Emerg Microbes Infect. 2021 Dec;10(1):1471-1480. (PMID: 34197273)
Nat Commun. 2024 Feb 20;15(1):1545. (PMID: 38378896)
Microorganisms. 2021 Nov 17;9(11):. (PMID: 34835497)
PLoS One. 2024 Dec 30;19(12):e0316466. (PMID: 39775564)
BMC Bioinformatics. 2018 Aug 29;19(1):307. (PMID: 30157759)
IJID Reg. 2024 May 01;11:100372. (PMID: 38799797)
Nat Methods. 2023 Nov;20(11):1661-1665. (PMID: 37735570)
Nucleic Acids Res. 2015 Feb 18;43(3):e15. (PMID: 25414349)
MMWR Morb Mortal Wkly Rep. 2019 Nov 22;68(46):1045-1049. (PMID: 31751325)
Grant Information: 2030-42000-055-000-D Agricultural Research Service
Contributed Indexing: Keywords: Salmonella Infantis; antimicrobial-resistant genes; mobile genetic elements; virulence factors
Substance Nomenclature: 0 (Virulence Factors)
0 (Anti-Bacterial Agents)
Entry Date(s): Date Created: 20260723 Date Completed: 20260902 Latest Revision: 20260903
Update Code: 20260903
PubMed Central ID: PMC13532305
DOI: 10.1128/spectrum.01827-25
PMID: 42489462
Βάση Δεδομένων: MEDLINE
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  Data: Mobile genetic elements-driven partitions of mega-plasmids resistome in Salmonella Infantis.
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  Data: <searchLink fieldCode="AU" term="%22Zhang+Y%22">Zhang Y</searchLink>; Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, California, USA.<br /><searchLink fieldCode="AU" term="%22Chu+M%22">Chu M</searchLink>; Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, California, USA.<br /><searchLink fieldCode="AU" term="%22Liao+Y-T%22">Liao Y-T</searchLink>; Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, California, USA.<br /><searchLink fieldCode="AU" term="%22Wu+VCH%22">Wu VCH</searchLink>; Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, California, USA.
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  Data: <searchLink fieldCode="MM" term="%22Salmonella+enterica%22">Salmonella enterica*</searchLink>/<searchLink fieldCode="MM" term="%22Salmonella+enterica+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Salmonella+enterica%22">Salmonella enterica*</searchLink>/<searchLink fieldCode="MM" term="%22Salmonella+enterica+drug+effects%22">drug effects</searchLink> <br /><searchLink fieldCode="MM" term="%22Plasmids%22">Plasmids*</searchLink>/<searchLink fieldCode="MM" term="%22Plasmids+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Interspersed+Repetitive+Sequences%22">Interspersed Repetitive Sequences*</searchLink><br /><searchLink fieldCode="MH" term="%22Virulence+Factors%22">Virulence Factors</searchLink>/<searchLink fieldCode="MH" term="%22Virulence+Factors+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Anti-Bacterial+Agents%22">Anti-Bacterial Agents</searchLink>/<searchLink fieldCode="MH" term="%22Anti-Bacterial+Agents+pharmacology%22">pharmacology</searchLink> ; <searchLink fieldCode="MH" term="%22Salmonella+Infections%22">Salmonella Infections</searchLink>/<searchLink fieldCode="MH" term="%22Salmonella+Infections+microbiology%22">microbiology</searchLink> ; <searchLink fieldCode="MH" term="%22Drug+Resistance%2C+Bacterial%22">Drug Resistance, Bacterial</searchLink>/<searchLink fieldCode="MH" term="%22Drug+Resistance%2C+Bacterial+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Salmonella%22">Salmonella</searchLink>/<searchLink fieldCode="MH" term="%22Salmonella+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Drug+Resistance%2C+Multiple%2C+Bacterial%22">Drug Resistance, Multiple, Bacterial</searchLink>/<searchLink fieldCode="MH" term="%22Drug+Resistance%2C+Multiple%2C+Bacterial+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Gene+Transfer%2C+Horizontal%22">Gene Transfer, Horizontal</searchLink> ; <searchLink fieldCode="MH" term="%22Humans%22">Humans</searchLink> ; <searchLink fieldCode="MH" term="%22Genome%2C+Bacterial%22">Genome, Bacterial</searchLink>
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  Data: Salmonella enterica serovar Infantis (S. Infantis) becomes the primary pathogen among the top Salmonella serotypes, contributing to numerous cases of foodborne illness annually in the United States. S. Infantis infection has spread rapidly worldwide, especially the clones with pESI-like plasmids. However, the underlying mechanisms regarding the transmission of S. Infantis, particularly mobile genetic elements (MGEs), mediated horizontal gene transfer, are limited. The objective of this study was to evaluate the relationship, if any, among MGEs, antibiotic-resistant genes (ARGs), and virulence factors (VFs) within S. Infantis via genomic analysis. A total of 91 S. Infantis complete genomes with high sequencing quality were selected for downstream bioinformatic analysis. The results showed that the majority of VFs were located in the bacterial chromosomes, while most ARGs were carried by S. Infantis mega-plasmids in an MGE-favored manner. Integrons and transposons were closely associated with certain ARGs, but prophages within mega-plasmids displayed a diverse ARG profile. Collectively, MGE-mediated horizontal gene transfer might lead to ARG acquisition by mega-plasmids, subsequently contributing to the resistome of S. Infantis. Our findings provide insights into the development of MGE-associated resistome in S. Infantis that could inform more effective prevention and intervention strategies to control this pathogen, further ensuring public health and safety.IMPORTANCEThe rapid emergence and transmission of antibiotic-resistant foodborne pathogens pose a significant risk to public health, necessitating the discovery of underlying mechanisms to control multidrug-resistant pathogens. Salmonella enterica serovar Infantis (S. Infantis) has become a pathogen of clinical and epidemiological relevance in recent years, ranking as the top prevalent serovar associated with foodborne illnesses and exhibiting resistance to several antibiotics. The current investigation of multidrug resistance (MDR) S. Infantis strains primarily emphasized the presence of mega-plasmids. However, the question of how mega-plasmids contribute to the transmission of antibiotic-resistant genes (ARG) is unaddressed. Utilizing the genomic characterization of S. Infantis complete genomes with high quality, our study revealed that the resistome of S. Infantis mega-plasmids-the primary ARG reservoirs of S. Infantis-followed a specific pattern of mobile genetic elements (MGEs). Monitoring the spread of MGE-carried ARGs within mega-plasmids should be considered in future surveillance.
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: The authors declare no conflict of interest.
– Name: Ref
  Label: References
  Group: RefInfo
  Data: Emerg Infect Dis. 2023 Aug;29(8):1634-1637. (PMID: <searchLink fieldCode="PM" term="%2237486207%22">37486207)</searchLink><br />Microb Genom. 2022 Jan;8(1):. (PMID: <searchLink fieldCode="PM" term="%2235072601%22">35072601)</searchLink><br />Environ Microbiol. 2014 Apr;16(4):977-94. (PMID: <searchLink fieldCode="PM" term="%2224320043%22">24320043)</searchLink><br />EFSA J. 2021 Apr 12;19(4):e06490. (PMID: <searchLink fieldCode="PM" term="%2233868492%22">33868492)</searchLink><br />BMC Genomics. 2019 Nov 15;20(1):870. (PMID: <searchLink fieldCode="PM" term="%2231730461%22">31730461)</searchLink><br />mSystems. 2016 Jun 21;1(3):. (PMID: <searchLink fieldCode="PM" term="%2227822532%22">27822532)</searchLink><br />Front Microbiol. 2021 Jul 23;12:649969. (PMID: <searchLink fieldCode="PM" term="%2234367079%22">34367079)</searchLink><br />BMC Genom Data. 2025 Feb 28;26(1):15. (PMID: <searchLink fieldCode="PM" term="%2240022005%22">40022005)</searchLink><br />Mol Biol Evol. 2021 Sep 27;38(10):4647-4654. (PMID: <searchLink fieldCode="PM" term="%2234320186%22">34320186)</searchLink><br />Int J Food Microbiol. 2020 Apr 16;319:108497. (PMID: <searchLink fieldCode="PM" term="%2231927155%22">31927155)</searchLink><br />Nucleic Acids Res. 2024 Jul 5;52(W1):W78-W82. (PMID: <searchLink fieldCode="PM" term="%2238613393%22">38613393)</searchLink><br />Nucleic Acids Res. 2016 Jul 8;44(W1):W16-21. (PMID: <searchLink fieldCode="PM" term="%2227141966%22">27141966)</searchLink><br />Mol Biol Evol. 2009 Jul;26(7):1641-50. (PMID: <searchLink fieldCode="PM" term="%2219377059%22">19377059)</searchLink><br />Front Microbiol. 2018 May 04;9:836. (PMID: <searchLink fieldCode="PM" term="%2229780368%22">29780368)</searchLink><br />J Clin Microbiol. 2015 May;53(5):1685-92. (PMID: <searchLink fieldCode="PM" term="%2225762776%22">25762776)</searchLink><br />Microorganisms. 2023 Feb 21;11(3):. (PMID: <searchLink fieldCode="PM" term="%2236985115%22">36985115)</searchLink><br />Antimicrob Agents Chemother. 2017 Jun 27;61(7):. (PMID: <searchLink fieldCode="PM" term="%2228483962%22">28483962)</searchLink><br />Poult Sci. 2024 Apr;103(4):103516. (PMID: <searchLink fieldCode="PM" term="%2238368739%22">38368739)</searchLink><br />PLoS One. 2024 Mar 14;19(3):e0299354. (PMID: <searchLink fieldCode="PM" term="%2238483966%22">38483966)</searchLink><br />Nucleic Acids Res. 2025 Jan 6;53(D1):D871-D877. (PMID: <searchLink fieldCode="PM" term="%2239470738%22">39470738)</searchLink><br />Prev Vet Med. 2025 Jan;234:106364. (PMID: <searchLink fieldCode="PM" term="%2239510009%22">39510009)</searchLink><br />Mol Microbiol. 2019 Feb;111(2):303-316. (PMID: <searchLink fieldCode="PM" term="%2230466179%22">30466179)</searchLink><br />Bioessays. 2017 Dec;39(12):. (PMID: <searchLink fieldCode="PM" term="%2228983932%22">28983932)</searchLink><br />Front Microbiol. 2020 Jan 21;10:3093. (PMID: <searchLink fieldCode="PM" term="%2232038541%22">32038541)</searchLink><br />Int J Food Microbiol. 2025 Mar 16;432:111090. (PMID: <searchLink fieldCode="PM" term="%2239919607%22">39919607)</searchLink><br />Curr Opin Microbiol. 2005 Aug;8(4):451-8. (PMID: <searchLink fieldCode="PM" term="%2216019256%22">16019256)</searchLink><br />Brief Funct Genomics. 2013 Jul;12(4):354-65. (PMID: <searchLink fieldCode="PM" term="%2223520178%22">23520178)</searchLink><br />Antimicrob Agents Chemother. 2014 Jul;58(7):3895-903. (PMID: <searchLink fieldCode="PM" term="%2224777092%22">24777092)</searchLink><br />Microorganisms. 2022 Jul 21;10(7):. (PMID: <searchLink fieldCode="PM" term="%2235889197%22">35889197)</searchLink><br />Microbiol Spectr. 2024 May 2;12(5):e0004724. (PMID: <searchLink fieldCode="PM" term="%2238546218%22">38546218)</searchLink><br />Microbiol Spectr. 2022 Dec 21;10(6):e0248122. (PMID: <searchLink fieldCode="PM" term="%2236250854%22">36250854)</searchLink><br />Emerg Microbes Infect. 2021 Dec;10(1):1471-1480. (PMID: <searchLink fieldCode="PM" term="%2234197273%22">34197273)</searchLink><br />Nat Commun. 2024 Feb 20;15(1):1545. (PMID: <searchLink fieldCode="PM" term="%2238378896%22">38378896)</searchLink><br />Microorganisms. 2021 Nov 17;9(11):. (PMID: <searchLink fieldCode="PM" term="%2234835497%22">34835497)</searchLink><br />PLoS One. 2024 Dec 30;19(12):e0316466. (PMID: <searchLink fieldCode="PM" term="%2239775564%22">39775564)</searchLink><br />BMC Bioinformatics. 2018 Aug 29;19(1):307. (PMID: <searchLink fieldCode="PM" term="%2230157759%22">30157759)</searchLink><br />IJID Reg. 2024 May 01;11:100372. (PMID: <searchLink fieldCode="PM" term="%2238799797%22">38799797)</searchLink><br />Nat Methods. 2023 Nov;20(11):1661-1665. (PMID: <searchLink fieldCode="PM" term="%2237735570%22">37735570)</searchLink><br />Nucleic Acids Res. 2015 Feb 18;43(3):e15. (PMID: <searchLink fieldCode="PM" term="%2225414349%22">25414349)</searchLink><br />MMWR Morb Mortal Wkly Rep. 2019 Nov 22;68(46):1045-1049. (PMID: <searchLink fieldCode="PM" term="%2231751325%22">31751325)</searchLink>
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