Genotypic analyses of IncHI2 plasmids from enteric bacteria

Algarni, Suad; Gudeta, Dereje D.; Han, Jing; Nayak, Rajesh; Foley, Steven L.

doi:10.1038/s41598-024-59870-2

Title: Genotypic analyses of IncHI2 plasmids from enteric bacteria

Journal Article · 28 April 2024 · Scientific Reports

DOI: https://doi.org/10.1038/s41598-024-59870-2 · OSTI ID:2471326

Algarni, Suad ^[1]; Gudeta, Dereje D. ^[1]; Han, Jing ^[1]; Nayak, Rajesh ^[1]; Foley, Steven L. ^[1]

US Food and Drug Administration (USFDA), Jefferson, AR (United States). National Center for Toxicological Research

Incompatibility (Inc) HI2 plasmids are large (typically > 200 kb), transmissible plasmids that encode antimicrobial resistance (AMR), heavy metal resistance (HMR) and disinfectants/biocide resistance (DBR). To better understand the distribution and diversity of resistance-encoding genes among IncHI2 plasmids, computational approaches were used to evaluate resistance and transfer-associated genes among the plasmids. Complete IncHI2 plasmid (N - 667) sequences were extracted from GenBank and analyzed using AMRFinderPlus, IntegronFinder and Plasmid Transfer Factor database. The most common IncHI2-carrying genera included Enterobacter (N = 209), Escherichia (N = 208), and Salmonella (N = 204). Resistance genes distribution was diverse, with plasmids from Escherichia and Salmonella showing general similarity in comparison to Enterobacter and other taxa, which grouped together. Plasmids from Enterobacter and other taxa had a higher prevalence of multiple mercury resistance genes and arsenic resistance gene, arsC, compared to Escherichia and Salmonella. For sulfonamide resistance, sul1 was more common among Enterobacter and other taxa, compared to sul2 and sul3 for Escherichia and Salmonella. Similar gene diversity trends were also observed for tetracyclines, quinolones, β-lactams, and colistin. Over 99% of plasmids carried at least 25 IncHI2-associated conjugal transfer genes. These findings highlight the diversity and dissemination potential for resistance across different enteric bacteria and value of computational-based approaches for the resistance-gene assessment.

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Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC); USFDA

Grant/Contract Number:: SC0014664

OSTI ID:: 2471326

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 14; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Colistin resistance genes mcr-1 to mcr-5, including a case of triple occurrence (mcr-1, -3 and -5), in Escherichia coli isolates from faeces of healthy pigs, cattle and poultry in Belgium, 2012–2016 Timmermans, Michaël; Wattiau, Pierre; Denis, Olivier International Journal of Antimicrobial Agents, Vol. 57, Issue 6 https://doi.org/10.1016/j.ijantimicag.2021.106350	journal	June 2021
High prevalence of multidrug-resistant Escherichia coli and first detection of IncHI2/IncX4-plasmid carrying mcr-1 E. coli in retail ready-to-eat foods in China Zhang, Shuhong; Huang, Yuanbin; Yang, Guangzhu International Journal of Food Microbiology, Vol. 355 https://doi.org/10.1016/j.ijfoodmicro.2021.109349	journal	October 2021
National prevalence estimates for resistant Enterobacteriaceae and Acinetobacter species in hospitalized patients in the United States Gupta, Vikas; Ye, Gang; Olesky, Melanie International Journal of Infectious Diseases, Vol. 85 https://doi.org/10.1016/j.ijid.2019.06.017	journal	August 2019
pST15-IncHI2 plasmids co-harboring mcr-9 and several other antibiotic resistance genes in heavy metal tolerant Enterobacter cloacae complex isolates from hospital infections Galetti, Renata; Andrade, Leonardo Neves; Sazinas, Pavelas Journal of Global Antimicrobial Resistance, Vol. 31 https://doi.org/10.1016/j.jgar.2022.09.002	journal	December 2022
The first description of the complete genome sequence of multidrug-resistant Salmonella enterica serovar monophasic Typhimurium (1,4,[5],12:i:-) isolate with the mcr-1.1 gene on IncHI2 found in pig in Poland Zając, Magdalena; Iwan, Ewelina; Skarżyńska, Magdalena Journal of Global Antimicrobial Resistance, Vol. 33 https://doi.org/10.1016/j.jgar.2023.04.008	journal	June 2023
Identification of plasmids by PCR-based replicon typing Carattoli, Alessandra; Bertini, Alessia; Villa, Laura Journal of Microbiological Methods, Vol. 63, Issue 3 https://doi.org/10.1016/j.mimet.2005.03.018	journal	December 2005
The complete nucleotide sequence of the resistance plasmid R478: defining the backbone components of incompatibility group H conjugative plasmids through comparative genomics Gilmour, Matthew W.; Thomson, Nicholas R.; Sanders, Mandy Plasmid, Vol. 52, Issue 3 https://doi.org/10.1016/j.plasmid.2004.06.006	journal	November 2004
Complete nucleotide sequence of pH11, an IncHI2 plasmid conferring multi-antibiotic resistance and multi-heavy metal resistance genes in a clinical Klebsiella pneumoniae isolate Zhai, Yao; He, Zilong; Kang, Yu Plasmid, Vol. 86 https://doi.org/10.1016/j.plasmid.2016.04.001	journal	July 2016
Identification of a novel lineage of plasmids within phylogenetically diverse subclades of IncHI2-ST1 plasmids Roy Chowdhury, Piklu; Fourment, Mathieu; DeMaere, Matthew Z. Plasmid, Vol. 102 https://doi.org/10.1016/j.plasmid.2019.03.002	journal	March 2019
Arsenical resistance in the IncHI2 plasmids Ryan, David; Colleran, Emer Plasmid, Vol. 47, Issue 3 https://doi.org/10.1016/s0147-619x(02)00012-4	journal	May 2002
Emergence of new IncHI2 multidrug-resistance plasmids carrying VIM-1 metallo-β-lactamase in Escherichia coli in Norway Marathe, Nachiket P.; Radisic, Vera; Salvà-Serra, Francisco The Lancet Microbe, Vol. 4, Issue 9 https://doi.org/10.1016/s2666-5247(22)00389-5	journal	September 2023
Full-length transcript characterization of SF3B1 mutation in chronic lymphocytic leukemia reveals downregulation of retained introns Tang, Alison D.; Soulette, Cameron M.; van Baren, Marijke J. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15171-6	journal	March 2020
Comparative genomic analysis of Colistin resistant Escherichia coli isolated from pigs, a human and wastewater on colistin withdrawn pig farm Khine, Nwai Oo; Wongsurawat, Thidathip; Jenjaroenpun, Piroon Scientific Reports, Vol. 13, Issue 1 https://doi.org/10.1038/s41598-023-32406-w	journal	March 2023
Co-spread of metal and antibiotic resistance within ST3-IncHI2 plasmids from E. coli isolates of food-producing animals Fang, Liangxing; Li, Xingping; Li, Liang Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25312	journal	May 2016
Escalating antimicrobial resistance among Enterobacteriaceae: focus on carbapenemases Lynch, Joseph P.; Clark, Nina M.; Zhanel, George G. Expert Opinion on Pharmacotherapy, Vol. 22, Issue 11 https://doi.org/10.1080/14656566.2021.1904891	journal	July 2021
Unique Class 1 Integron and Multiple Resistance Genes Co-located on IncHI2 Plasmid Is Associated with the Emerging Multidrug Resistance of Salmonella Indiana Isolated from Chicken in China Lai, Jing; Wang, Yang; Shen, Jianzhong Foodborne Pathogens and Disease, Vol. 10, Issue 7 https://doi.org/10.1089/fpd.2012.1455	journal	July 2013
First Detection of bla_NDM-1-Haboring IncHI2 Plasmid in Escherichia coli Strain Isolated from Goose in China Fu, Shasha; Jin, Shanshan; Ge, Haojie Foodborne Pathogens and Disease, Vol. 20, Issue 6 https://doi.org/10.1089/fpd.2022.0071	journal	June 2023
Antibiotic Resistance in Salmonella from Retail Foods of Animal Origin and Its Association with Disinfectant and Heavy Metal Resistance Deng, Wenwen; Quan, Yuan; Yang, Shengzhi Microbial Drug Resistance, Vol. 24, Issue 6 https://doi.org/10.1089/mdr.2017.0127	journal	July 2018
Escherichia fergusonii Harboring IncHI2 Plasmid Containing mcr-1 Gene: A Novel Reservoir for Colistin Resistance in Brazil Pontes, Leilane da Silva; Pimenta, Ramon; Silveira, Melise Chaves Microbial Drug Resistance https://doi.org/10.1089/mdr.2020.0041	journal	October 2020
Co-Occurrence ofmcr-1andqnrS1on an IncHI2 Plasmid in Clinical Isolates ofSalmonellaTyphimurium in Spain Trujillo-Soto, Teresa; Machuca, Jesús; Arca-Suárez, Jorge Vector-Borne and Zoonotic Diseases, Vol. 19, Issue 9 https://doi.org/10.1089/vbz.2018.2398	journal	September 2019
Curation, integration and visualization of bacterial virulence factors in PATRIC Mao, Chunhong; Abraham, David; Wattam, Alice R. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu631	journal	September 2014
Roary: rapid large-scale prokaryote pan genome analysis Page, Andrew J.; Cummins, Carla A.; Hunt, Martin Bioinformatics, Vol. 31, Issue 22 https://doi.org/10.1093/bioinformatics/btv421	journal	July 2015
Detection of mobile genetic elements associated with antibiotic resistance in Salmonella enterica using a newly developed web tool: MobileElementFinder Johansson, Markus H. K.; Bortolaia, Valeria; Tansirichaiya, Supathep Journal of Antimicrobial Chemotherapy, Vol. 76, Issue 1 https://doi.org/10.1093/jac/dkaa390	journal	October 2020
Co-occurrence of the blaVIM-1 and blaSHV-12 genes on an IncHI2 plasmid of an Escherichia coli isolate recovered from German livestock Pauly, N.; Hammerl, J. A.; Schwarz, S. Journal of Antimicrobial Chemotherapy, Vol. 76, Issue 2 https://doi.org/10.1093/jac/dkaa436	journal	November 2020
Co-localization of carbapenem (blaOXA-162) and colistin (mcr-1) resistance genes on a transferable IncHI2 plasmid in Escherichia coli of chicken origin Bortolaia, Valeria; Ronco, Troels; Romascu, Luminita Journal of Antimicrobial Chemotherapy, Vol. 76, Issue 11 https://doi.org/10.1093/jac/dkab285	journal	August 2021
Plasmid double locus sequence typing for IncHI2 plasmids, a subtyping scheme for the characterization of IncHI2 plasmids carrying extended-spectrum β-lactamase and quinolone resistance genes García-Fernández, Aurora; Carattoli, Alessandra Journal of Antimicrobial Chemotherapy, Vol. 65, Issue 6 https://doi.org/10.1093/jac/dkq101	journal	March 2010
Evolution of IncHI2 plasmids via acquisition of transposons carrying antibiotic resistance determinants Cain, A. K.; Hall, R. M. Journal of Antimicrobial Chemotherapy, Vol. 67, Issue 5 https://doi.org/10.1093/jac/dks004	journal	February 2012
Identification of acquired antimicrobial resistance genes Zankari, E.; Hasman, H.; Cosentino, S. Journal of Antimicrobial Chemotherapy, Vol. 67, Issue 11 https://doi.org/10.1093/jac/dks261	journal	July 2012
WGS accurately predicts antimicrobial resistance in Escherichia coli Tyson, Gregory H.; McDermott, Patrick F.; Li, Cong Journal of Antimicrobial Chemotherapy, Vol. 70, Issue 10 https://doi.org/10.1093/jac/dkv186	journal	July 2015
Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae Rozwandowicz, M.; Brouwer, M. S. M.; Fischer, J. Journal of Antimicrobial Chemotherapy, Vol. 73, Issue 5 https://doi.org/10.1093/jac/dkx488	journal	January 2018
Validating the AMRFinder Tool and Resistance Gene Database by Using Antimicrobial Resistance Genotype-Phenotype Correlations in a Collection of Isolates Feldgarden, Michael; Brover, Vyacheslav; Haft, Daniel H. Antimicrobial Agents and Chemotherapy, Vol. 63, Issue 11 https://doi.org/10.1128/AAC.00483-19	journal	August 2019
Resistance Plasmid Families in Enterobacteriaceae Carattoli, Alessandra Antimicrobial Agents and Chemotherapy, Vol. 53, Issue 6 https://doi.org/10.1128/AAC.01707-08	journal	June 2009
Molecular Characterization of IMP-1-Producing Enterobacter cloacae Complex Isolates in Tokyo Aoki, Kotaro; Harada, Sohei; Yahara, Koji Antimicrobial Agents and Chemotherapy, Vol. 62, Issue 3 https://doi.org/10.1128/AAC.02091-17	journal	March 2018
In Silico Detection and Typing of Plasmids using PlasmidFinder and Plasmid Multilocus Sequence Typing Carattoli, Alessandra; Zankari, Ea; García-Fernández, Aurora Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 7 https://doi.org/10.1128/AAC.02412-14	journal	April 2014
Plasmid Replicon Typing of Commensal and Pathogenic Escherichia coli Isolates Johnson, Timothy J.; Wannemuehler, Yvonne M.; Johnson, Sara J. Applied and Environmental Microbiology, Vol. 73, Issue 6 https://doi.org/10.1128/AEM.02171-06	journal	March 2007
The Changing Face of the Family Enterobacteriaceae (Order: “ Enterobacterales ”): New Members, Taxonomic Issues, Geographic Expansion, and New Diseases and Disease Syndromes Janda, J. Michael; Abbott, Sharon L. Clinical Microbiology Reviews, Vol. 34, Issue 2 https://doi.org/10.1128/CMR.00174-20	journal	March 2021
The Evolution of Class 1 Integrons and the Rise of Antibiotic Resistance Gillings, Michael; Boucher, Yan; Labbate, Maurizio Journal of Bacteriology, Vol. 190, Issue 14 https://doi.org/10.1128/JB.00152-08	journal	July 2008
Temperature-Dependent Conjugative Transfer of R27: Role of Chromosome- and Plasmid-Encoded Hha and H-NS Proteins Forns, Núria; Baños, Rosa C.; Balsalobre, Carlos Journal of Bacteriology, Vol. 187, Issue 12 https://doi.org/10.1128/JB.187.12.3950-3959.2005	journal	June 2005
Dissemination of Extended-Spectrum-β-Lactamase-Producing Enterobacter cloacae Complex from a Hospital to the Nearby Environment in Guadeloupe (French West Indies): ST114 Lineage Coding for a Successful IncHI2/ST1 Plasmid Pot, Matthieu; Guyomard-Rabenirina, Stéphanie; Couvin, David Antimicrobial Agents and Chemotherapy, Vol. 65, Issue 3 https://doi.org/10.1128/aac.02146-20	journal	February 2021
Phage inhibition, colicin resistance, and tellurite resistance are encoded by a single cluster of genes on the IncHI2 plasmid R478 Whelan, K. F.; Colleran, E.; Taylor, D. E. Journal of Bacteriology, Vol. 177, Issue 17 https://doi.org/10.1128/jb.177.17.5016-5027.1995	journal	September 1995
Plasmid incompatibility Novick, R. P. Microbiological Reviews, Vol. 51, Issue 4 https://doi.org/10.1128/mr.51.4.381-395.1987	journal	December 1987
IncHI2 Plasmid Encoding bla _CTX-M-55 and mcr-1.1 in Salmonella enterica SE20-C72-2 and Escherichia coli EC20-C72-1 Isolates from the Edible River Fish Anabas testudineus Nakayama, Tatsuya; Yamamoto, Shiori; Ohata, Natsuki Microbiology Resource Announcements, Vol. 12, Issue 7 https://doi.org/10.1128/mra.00149-23	journal	July 2023
Complete Genome Sequence of a Colistin-Susceptible Salmonella enterica Serovar Minnesota Strain Harboring mcr-9 on an IncHI2/IncHI2A Plasmid, Isolated from Chicken Meat Alzahrani, Khaloud O.; Alshdokhi, Elaf A.; Mujallad, Mohammed I. Microbiology Resource Announcements, Vol. 10, Issue 45 https://doi.org/10.1128/mra.00826-21	journal	November 2021
A Trade-Off for Maintenance of Multidrug-Resistant IncHI2 Plasmids in Salmonella enterica Serovar Typhimurium through Adaptive Evolution Zhang, Jin-Fei; Fang, Liang-Xing; Chang, Man-Xia mSystems, Vol. 7, Issue 5 https://doi.org/10.1128/msystems.00248-22	journal	October 2022
BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons Alikhan, Nabil-Fareed; Petty, Nicola K.; Ben Zakour, Nouri L. BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-402	journal	August 2011
DNA Sequence Analysis of Plasmids from Multidrug Resistant Salmonella enterica Serotype Heidelberg Isolates Han, Jing; Lynne, Aaron M.; David, Donna E. PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0051160	journal	December 2012
Healthcare-associated infections caused by chlorhexidine-tolerant Serratia marcescens carrying a promiscuous IncHI2 multi-drug resistance plasmid in a veterinary hospital Allen, Joanne L.; Doidge, Nicholas P.; Bushell, Rhys N. PLOS ONE, Vol. 17, Issue 3 https://doi.org/10.1371/journal.pone.0264848	journal	March 2022
Development of an antimicrobial resistance plasmid transfer gene database for enteric bacteria Algarni, Suad; Foley, Steven L.; Tang, Hailin Frontiers in Bioinformatics, Vol. 3 https://doi.org/10.3389/fbinf.2023.1279359	journal	November 2023
oqxAB-Positive IncHI2 Plasmid pHXY0908 Increase Salmonella enterica Serotype Typhimurium Strains Tolerance to Ciprofloxacin Lian, Xinlei; Wang, Xiran; Liu, Xiao Frontiers in Cellular and Infection Microbiology, Vol. 9 https://doi.org/10.3389/fcimb.2019.00242	journal	July 2019
Genomic Characterization of Two Escherichia fergusonii Isolates Harboring mcr-1 Gene From Farm Environment Liu, Ruishan; Xu, Hao; Guo, Xiaobing Frontiers in Cellular and Infection Microbiology, Vol. 12 https://doi.org/10.3389/fcimb.2022.774494	journal	May 2022
IncHI2 Plasmids Are Predominant in Antibiotic-Resistant Salmonella Isolates Chen, Wenyao; Fang, Tingzi; Zhou, Xiujuan Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01566	journal	September 2016
Transmissible ST3-IncHI2 Plasmids Are Predominant Carriers of Diverse Complex IS26-Class 1 Integron Arrangements in Multidrug-Resistant Salmonella Zhao, Hang; Chen, Wenyao; Xu, Xuebin Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02492	journal	October 2018
Emergence of IncHI2 Plasmids With Mobilized Colistin Resistance (mcr)-9 Gene in ESBL-Producing, Multidrug-Resistant Salmonella Typhimurium and Its Monophasic Variant ST34 From Food-Producing Animals in Italy Diaconu, Elena Lavinia; Alba, Patricia; Feltrin, Fabiola Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.705230	journal	July 2021
In silico analyses of diversity and dissemination of antimicrobial resistance genes and mobile genetics elements, for plasmids of enteric pathogens Algarni, Suad; Han, Jing; Gudeta, Dereje D. Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.1095128	journal	January 2023
The Dynamics of the Antimicrobial Resistance Mobilome of Salmonella enterica and Related Enteric Bacteria Algarni, Suad; Ricke, Steven C.; Foley, Steven L. Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.859854	journal	March 2022
The Intestinal Carriage of Plasmid-Mediated Colistin-Resistant Enterobacteriaceae in Tertiary Care Settings Tkadlec, Jan; Kalova, Alzbeta; Brajerova, Marie Antibiotics, Vol. 10, Issue 3 https://doi.org/10.3390/antibiotics10030258	journal	March 2021
Genomic Analysis of a mcr-9.1-Harbouring IncHI2-ST1 Plasmid from Enterobacter ludwigii Isolated in Fish Farming Manageiro, Vera; Salgueiro, Vanessa; Rosado, Tânia Antibiotics, Vol. 11, Issue 9 https://doi.org/10.3390/antibiotics11091232	journal	September 2022
IntegronFinder 2.0: Identification and Analysis of Integrons across Bacteria, with a Focus on Antibiotic Resistance in Klebsiella Néron, Bertrand; Littner, Eloi; Haudiquet, Matthieu Microorganisms, Vol. 10, Issue 4 https://doi.org/10.3390/microorganisms10040700	journal	March 2022
Genomic Insights into a Colistin-Resistant Uropathogenic Escherichia coli Strain of O23:H4-ST641 Lineage Harboring mcr-1.1 on a Conjugative IncHI2 Plasmid from Egypt Zakaria, Azza S.; Edward, Eva A.; Mohamed, Nelly M. Microorganisms, Vol. 9, Issue 4 https://doi.org/10.3390/microorganisms9040799	journal	April 2021

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