Horizontal Transfer of the Salmonella enterica Serovar Infantis Resistance and Virulence Plasmid pESI to the Gut Microbiota of Warm-Blooded Hosts

mBio - Tập 7 Số 5 - 2016
Gili Aviv1,2,3, Galia Rahav2,3, Ohad Gal‐Mor1,2,3
1Department of Clinical Microbiology and Immunology, Tel Aviv University, Tel Aviv, Israel
2Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
3The Infectious Diseases Research Laboratory, Sheba Medical Center, Tel-Hashomer, Israel

Tóm tắt

ABSTRACT Salmonella enterica serovar Infantis is one of the prevalent salmonellae worldwide. Recently, we showed that the emergence of S . Infantis in Israel was facilitated by the acquisition of a unique megaplasmid (pESI) conferring multidrug resistance and increased virulence phenotypes. Here we elucidate the ecology, transmission properties, and regulation of pESI. We show that despite its large size (~280 kb), pESI does not impose a significant metabolic burden in vitro and that it has been recently fixed in the domestic S . Infantis population. pESI conjugation and the transcription of its pilus ( pil ) genes are inhibited at the ambient temperature (27°C) and by ≥1% bile but increased under temperatures of 37 to 41°C, oxidative stress, moderate osmolarity, and the microaerobic conditions characterizing the intestinal environment of warm-blooded animals. The pESI-encoded protein TraB and the oxygen homeostasis regulator Fnr were identified as transcriptional regulators of pESI conjugation. Using the mouse model, we show that following S . Infantis infection, pESI can be horizontally transferred to the gut microbiota, including to commensal Escherichia coli strains. Possible transfer, but not persistence, of pESI was also observed into Gram-positive mouse microbiota species, especially Lactobacillus reuteri . Moreover, pESI was demonstrated to further disseminate from gut microbiota to S. enterica serovar Typhimurium, in the context of gastrointestinal infection. These findings exhibit the ability of a selfish clinically relevant megaplasmid to distribute to and from the microbiota and suggest an overlooked role of the microbiota as a reservoir of mobile genetic elements and intermediator in the spread of resistance and virulence genes between commensals and pathogenic bacteria. IMPORTANCE Plasmid conjugation plays a key role in microbial evolution, enabling the acquisition of new phenotypes, including resistance and virulence. Salmonella enterica serovar Infantis is one of the ubiquitous salmonellae worldwide and a major cause of foodborne infections. Previously, we showed that the emergence of S . Infantis in Israel has involved the acquisition of a unique megaplasmid (pESI) conferring multidrug resistance and increased virulence phenotypes. Recently, the emergence of another S . Infantis strain carrying a pESI-like plasmid was identified in Italy, suggesting that the acquisition of pESI may be common to different emergent S . Infantis populations globally. Transmission of this plasmid to other strains or bacterial species is an alarming scenario. Understanding the ecology, regulation, and transmission properties of clinically relevant plasmids and the role of the microbiota in their spreading offers a new mechanism explaining the emergence of new pathogenic and resistant biotypes and may assist in the development of appropriate surveillance and prevention measures.

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Tài liệu tham khảo

10.3201/eid1205.050854

10.1086/650733

10.1128/mBio.00579-12

10.1016/S0966-842X(01)02293-4

Crim SM, Griffin PM, Tauxe R, Marder EP, Gilliss D, Conquist AB, Cartter M, Tobin-D’Angelo M, Blythe D, Smith K, Lathrop S, Zansky S, Cieslak PR, Dunn J, Holt KG, Wolpert B, Henao OL, Centers for Disease Control and Prevention. 2015. Preliminary incidence and trends of infection with pathogens transmitted commonly through food—Foodborne Diseases Active Surveillance Network, 10 U.S. sites, 2006–2014. MMWR Morb Mortal Wkly Rep 64:495–499.

ECDC. 2009. Annual epidemiological report on communicable diseases in Europe 2009. European Centre for Disease Prevention and Control, Stockholm, Sweden.

10.1111/1462-2920.12351

10.3201/eid1611.100100

10.1371/journal.pone.0144802

10.1016/S0966-842X(00)01703-0

10.1007/s000180050021

10.1128/MMBR.00020-10

10.1038/nrmicro2382

10.1128/IAI.00127-11

10.1016/j.jbiotec.2005.11.014

10.1073/pnas.1107254109

10.1152/jappl.1997.83.1.204

10.3923/ijps.2008.223.233

10.1128/JB.184.2.444-451.2002

10.1046/j.1365-2958.2002.02981.x

10.1534/genetics.109.109918

10.1146/annurev.micro.53.1.495

10.3109/07853890109002075

10.1046/j.1365-2958.1997.4731841.x

10.1093/genetics/161.4.1373

10.1016/j.bbamcr.2013.12.019

10.2217/fmb.10.70

10.1016/j.cub.2015.06.024

10.1038/ncomms7845

10.1128/jb.175.16.5035-5042.1993

10.1099/00221287-133-12-3279

10.1128/JB.00726-06

10.1099/mic.0.28256-0

10.1128/JB.01626-07

10.1016/0165-1110(90)90023-5

10.1073/pnas.96.8.4586

10.1146/annurev-micro-090110-102830

10.1038/nature08821

10.1128/jb.88.2.322-328.1964

10.1016/j.ygeno.2012.07.012

10.1128/iai.24.3.982-984.1979

10.1128/jb.173.21.6705-6708.1991

10.1016/S0147-619X(03)00044-1

Li W, Shen M, Jiao R, Zhao G. 1999. Conjugational actinomycetes of plasmid RSF101 from Escherichia coli to the rare actinomycetes of Nocardia asteriodes and Streptoverticillum caespitosus. Acta Microbiol Sin 39:376–380. (In Chinese.)

10.1007/PL00006802

10.1128/JCM.37.9.3062-3064.1999

10.1093/jac/dkr547

10.3201/eid1606.091671

10.1093/jac/dkm327

10.1016/j.tim.2004.07.004

Summanen P, Baron EJ, Citron DM, Strong CA, Wexler HM, Finegold SM. 1993. Wadsworth anaerobic bacteriology manual, 5th ed. Star Publishing Co, Redwood City, CA.

10.1089/fpd.2006.3.59

10.1128/IAI.00468-15

10.1186/1471-2199-7-31

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