IncF ColV plasmids are important plasmid incompatibility group that are currently restricted to the Enterobacteriaceae. These plasmids carry an important repertoire of virulence-associated genes (VAGs) that contribute to the ability of avian pathogenic Escherichia coli to cause disease in poultry. VAGs found on ColV plasmids have also been linked to urosepsis and meningitis in humans but the mechanisms that elicit these disease conditions are not well understood. Recently we described the sequence of a ColV plasmid pSDJ2009-52F that carried the typical repertoire of VAGs and a complex resistance gene locus flanked by IS26, an insertion element that plays an important role in mobilizing antibiotic resistance genes on plasmids and genomic islands. We recovered complete ColV-like plasmid sequences from public databases that shared >80% sequence identity with pSDJ2009-52F in geographically diverse regions of the world over a 20-year timeframe. Previously we noted that pSDJ2009-52F carries a unique genetic signature in the class 1 integron within the complex resistance locus that was presumably created by the action of IS26. Here we show that most ColV-like plasmids that are closely related to pSDJ2009-52F also carry the same signature. Our studies provide insight into how these signature-bearing plasmids and the mobile genetic elements they carry traffic between E. coli sequence types over large geographic distances.
Get full access to this article
View all access options for this article.
References
1.
VilaJ., Sáez-LópezE., JohnsonJ.R, RömlingU., DobrindtU., CantónR., GiskeC.G, NaasT., CarattoliA., Martínez-MedinaM., BoschJ., RetamarP., Rodríguez-BañoJ, BaqueroF., and SotoS.M.. 2016. Escherichia coli: an old friend with new tidings. FEMS Microbiol. Rev. 40:437–463.
2.
FangL.X., LiX.P, DengG.H, LiS.M, YangR.S, WuZ.W, LiaoX.P, SunJ., and LiuY.H.. 2018. High genetic plasticity in multidrug-resistant sequence type 3-IncHI2 plasmids revealed by sequence comparison and phylogenetic analysis. Antimicrob. Agents Chemother. 62:pii: e02068-17.
3.
VenturiniC., BeatsonS.A, DjordjevicS.P, and WalkerM.J.. 2010. Multiple antibiotic resistance gene recruitment onto the enterohemorrhagic Escherichia coli virulence plasmid. FASEB J. 24:1160–1166.
4.
VenturiniC., HassanK.A, Roy ChowdhuryP., PaulsenI.T, WalkerM.J, and DjordjevicS.P.. 2013. Sequences of two related multiple antibiotic resistance virulence plasmids sharing a unique IS26-related molecular signature isolated from different Escherichia coli pathotypes from different hosts. PLoS One. 8:e78862.
5.
WangX., HaoH., XuZ., ZhengH., LiuC., WeiL., ZhangR., BiD., ChenH., and TanC.. 2014. Plasmid-mediated multidrug resistance and virulence in an avian pathogenic Escherichia coli strain isolated in China. J. Glob. Antimicrob. Resist. 2:57–58.
6.
JacksonR.W., VinatzerB., ArnoldD.L, DorusS., and MurilloJ.. 2011. The influence of the accessory genome on bacterial pathogen evolution. Mob. Genet. Elements. 1:55–65.
7.
JohnsonT.J., ThorsnessJ.L, AndersonC.P, LynneA.M, FoleyS.L, HanJ., FrickeW.F, McDermottP.F, WhiteD.G, KhatriM., StellA.L, FloresC., and SingerR.S.. 2010. Horizontal gene transfer of a ColV plasmid has resulted in a dominant avian clonal type of Salmonella enterica serovar Kentucky. PLoS One, 5:e15524.
8.
McKinnonJ., Roy ChowdhuryP., and DjordjevicS.P.. 2018. Genomic analysis of multidrug-resistant Escherichia coli ST58 causing urosepsis. Int. J. Antimicrob. Agents. 52:430–435.
9.
ZhengB., YuX., XuH., GuoL., ZhangJ., HuangC., ShenP., JiangX., XiaoY., and LiL.. 2017. Complete genome sequencing and genomic characterization of two Escherichia coli strains co-producing MCR-1 and NDM-1 from bloodstream infection. Sci. Rep. 7:17885.
10.
KawamuraK., SugawaraT., MatsuoN., HayashiK., NorizukiC., TamaiK., KondoT., and ArakawaY.. 2017. Spread of CTX-type extended-spectrum beta-lactamase-producing Escherichia coli isolates of epidemic clone B2-O25-ST131 among dogs and cats in Japan. Microb. Drug Resist. 23:1059–1066.
11.
JohnsonT.J., SiekK.E, JohnsonS.J, and NolanL.K.. 2006. DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J. Bacteriol. 188:745–758.
12.
MoranR.A., HoltK.E, and HallR.M.. 2016. pCERC3 from a commensal ST95 Escherichia coli: A ColV virulence-multiresistance plasmid carrying a sul3-associated class 1 integron. Plasmid, 84–85:11–19.
13.
Fernandez-BerosM.E., KisselV., LiorH., and CabelloF.C.. 1990. Virulence-related genes in ColV plasmids of Escherichia coli isolated from human blood and intestines. J. Clin. Microbiol. 28:742–746.
14.
PeigneC., BidetP., Mahjoub-MessaiF., PlainvertC., BarbeV., MedigueC., FrapyE., NassifX., DenamurE., BingenE., and BonacorsiS.. 2009. The plasmid of Escherichia coli strain S88 (O45:K1:H7) that causes neonatal meningitis is closely related to avian pathogenic E. coli plasmids and is associated with high-level bacteremia in a neonatal rat meningitis model. Infect. Immun. 77:2272–2284.
15.
LemaitreC., BidetP., BenoistJ.F, SchlemmerD., SobralE., d'HumieresC., and BonacorsiS.. 2014. The ssbL gene harbored by the ColV plasmid of an Escherichia coli neonatal meningitis strain is an auxiliary virulence factor boosting the production of siderophores through the shikimate pathway. J. Bacteriol. 196:1343–1349.
16.
Zhu GeX., JiangJ., PanZ., HuL., WangS., WangH., LeungF.C, DaiJ., and FanH.. 2014. Comparative genomic analysis shows that avian pathogenic Escherichia coli isolate IMT5155 (O2:K1:H5; ST complex 95, ST140) shares close relationship with ST95 APEC O1:K1 and human ExPEC O18:K1 strains. PLoS One, 9:e112048.
17.
CainA.K., LiuX., DjordjevicS.P, and HallR.M.. 2010. Transposons related to Tn1696 in IncHI2 plasmids in multiply antibiotic resistant Salmonella enterica serovar Typhimurium from Australian animals. Microb. Drug Resist. 16:197–202.
18.
HarmerC.J., MoranR.A, and HallR.M.. 2014. Movement of IS26-associated antibiotic resistance genes occurs via a translocatable unit that includes a single IS26 and preferentially inserts adjacent to another IS26. mBio, 5:e01801-14.
19.
YauS., LiuX., DjordjevicS.P, and HallR.M.. 2010. RSF1010-like plasmids in Australian Salmonella enterica serovar Typhimurium and origin of their sul2-strA-strB antibiotic resistance gene cluster. Microb. Drug Resist. 16:249–252.
20.
DawesF.E., KuzevskiA., BettelheimK.A, HornitzkyM.A, DjordjevicS.P, and WalkerM.J.. 2010. Distribution of class 1 integrons with IS26-mediated deletions in their 3′-conserved segments in Escherichia coli of human and animal origin. PLoS One, 5:e12754.
21.
ReidC.J., WyrschE.R, Roy ChowdhuryP., ZingaliT., LiuM., DarlingA.E, ChapmanT.A, and DjordjevicS.P.. 2017. Porcine commensal Escherichia coli: a reservoir for class 1 integrons associated with IS26. Microb. Genom. 3:e000143.
22.
Roy ChowdhuryP., CharlesI.G, and DjordjevicS.P.. 2015. A role for Tn6029 in the evolution of the complex antibiotic resistance gene loci in genomic island 3 in enteroaggregative hemorrhagic Escherichia coli O104:H4. PLoS One, 10:e0115781.
23.
Roy ChowdhuryP., McKinnonJ., LiuM., and DjordjevicS.P. 2019. Multidrug resistant uropathogenic Escherichia coli. ST405 with a novel, composite IS26 transposon in a unique chromosomal location. Front. Microbiol. 9: , 3212.
24.
CumminsM.L., ReidC., Roy ChowdhuryP., BushnellR.N, EsbertN., TivendaleK.A, NoormohammadiA.H, IslamS., MarendaM.S, BrowningG.F, MarkhamP.F, and DjordjevicS.P. 2019. Whole genome sequence analysis of Australian avian pathogenic E. coli. that carry the class 1 integrase gene. Microb. Genom. 5. DOI: 10.1099/mgen.0.00, 0250.
25.
DahmenS., MetayerV., GayE., MadecJ.Y, and HaenniM.. 2013. Characterization of extended-spectrum beta-lactamase (ESBL)-carrying plasmids and clones of Enterobacteriaceae causing cattle mastitis in France. Vet. Microbiol. 162:793–799.
26.
WuG., EhrichtR., MafuraM., StokesM., SmithN., PritchardG.C, and WoodwardM.J.. 2012. Escherichia coli isolates from extraintestinal organs of livestock animals harbour diverse virulence genes and belong to multiple genetic lineages. Vet. Microbiol. 160:197–206.
27.
BlaakH., HamidjajaR.A, van HoekA.H, de HeerL., de Roda HusmanA.M, and SchetsF.M.. 2014. Detection of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli on flies at poultry farms. Appl. Environ. Microbiol. 80:239–246.
28.
SacramentoA.G., FernandesM.R, SelleraF.P, MunozM.E, VivasR., DolabellaS.S, and LincopanN.. 2018. Genomic analysis of MCR-1 and CTX-M-8 co-producing Escherichia coli ST58 isolated from a polluted mangrove ecosystem in Brazil. J. Glob. Antimicrob. Resist. 15:288–289.
29.
DolejskaM., MasarikovaM., DobiasovaH., JamborovaI., KarpiskovaR., HavlicekM., CarlileN., PriddelD., CizekA., and LiterakI.. 2016. High prevalence of Salmonella and IMP-4-producing Enterobacteriaceae in the silver gull on Five Islands, Australia. J. Antimicrob. Chemother. 71:63–70.
30.
TreangenT.J., OndovB.D, KorenS., and PhillippyA.M.. 2014. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 15:524.
31.
BouckaertR., HeledJ., KuhnertD., VaughanT., WuC.H, XieD., SuchardM.A, RambautA., and DrummondA.J.. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10:e1003537.
32.
DucheneS., HoltK.E, WeillF.X, Le HelloS., HawkeyJ., EdwardsD.J, FourmentM., and HolmesE.C.. 2016. Genome-scale rates of evolutionary change in bacteria. Microb. Genom. 2:e000094.
33.
AlikhanN., PettyN.K, Ben ZakourN.L, and BeatsonS.A.. 2011. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom. 12:402.
34.
ChoiY., and ChanA.P.. 2015. PROVEAN web server: a tool to predict the functional effect of amino acid substitutions and indels. Bioinformatics, 31:2745–2747.
35.
RozwandowiczM., BrouwerM.S.M, FischerJ., WagenaarJ.A, Gonzalez-ZornB., GuerraB., MeviusD.J, and HordijkJ.. 2018. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J. Antimicrob. Chemother. 73:1121–1137.
36.
PitoutJ.D., and DeVinneyR.. 2017. Escherichia coli ST131: a multidrug-resistant clone primed for global domination. F1000Res 6:pii: F1000 Faculty Rev-195.
37.
GillingsM.R., GazeW.H, PrudenA., SmallaK., TiedjeJ.M, and ZhuY.G.. 2015. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 9:1269–1279.
38.
LiebertC.A., HallR.M, and SummersA.O.. 1999. Transposon Tn21, flagship of the floating genome. Microbiol Mol Biol Rev. 63:507–522.
Adams-SapperS., DiepB.A, Perdreau-RemingtonF., and RileyL.W.. 2013. Clonal composition and community clustering of drug-susceptible and -resistant Escherichia coli isolates from bloodstream infections. Antimicrob. Agents Chemother. 57:490–497.
41.
Heidemann OlsenR., BisgaardM., ChristensenJ.P, KabellS., and ChristensenH.. 2016. Pathology and molecular characterization of Escherichia coli associated with the Avian Salpingitis-Peritonitis Disease Syndrome. Avian Dis. 60:1–7.
42.
MoraA., VisoS., LópezC., AlonsoM.P, García-GarroteF., DabhiG., MamaniR., HerreraA., MarzoaJ., BlancoM., BlancoJ.E, Moulin-SchouleurM., SchoulerC., and BlancoJ.. 2013. Poultry as reservoir for extraintestinal pathogenic Escherichia coli O45:K1:H7-B2-ST95 in humans. Vet. Microbiol. 167:506–512.
43.
NandanwarN., JanssenT., KuhlM., AhmedN., EwersC., and WielerL.H.. 2014. Extraintestinal pathogenic Escherichia coli (ExPEC) of human and avian origin belonging to sequence type complex 95 (STC95) portray indistinguishable virulence features. Int. J. Med. Microbiol. 304:835–842.
44.
DanzeisenJ.L., WannemuehlerY., NolanL.K, and JohnsonT.J.. 2013. Comparison of multilocus sequence analysis and virulence genotyping of Escherichia coli from live birds, retail poultry meat, and human extraintestinal infection. Avian Dis. 57:104–108.
45.
Leverstein-van HallM.A., DierikxC.M, Cohen StuartJ., VoetsG.M, van den MunckhofM.P, van Essen-ZandbergenA., PlatteelT., FluitA.C, van de Sande-BruinsmaN., ScharingaJ., BontenM.J, MeviusD.J, and NationalEsg. 2011. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin. Microbiol. Infect. 17:873–880.
46.
LiuC.M., SteggerM., AzizM., JohnsonT.J, WaitsK., NordstromL., GauldL., WeaverB., RollandD., StathamS., HorwinskiJ., SariyaS., DavisG.S, SokurenkoE., KeimP., JohnsonJ.R, and PriceL.B.. 2018. Escherichia coli ST131-H22 as a foodborne uropathogen. mBio, 9:pii: e00470-18.
47.
MalutaR.P., LogueC.M, CasasM.R, MengT., GuastalliE.A, RojasT.C, MontelliA.C, SadatsuneT., de Carvalho RamosM., NolanL.K, and da SilveiraW.D. 2014. Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS One, 9:e10. 5016.
48.
MoranR.A., and HallR.M.. 2017. Analysis of pCERC7, a small antibiotic resistance plasmid from a commensal ST131 Escherichia coli, defines a diverse group of plasmids that include various segments adjacent to a multimer resolution site and encode the same NikA relaxase accessory protein enabling mobilisation. Plasmid, 89:42–48.
49.
MangesA.R., MendeK., MurrayC.K, JohnstonB.D, SokurenkoE.V, TchesnokovaV., and JohnsonJ.R.. 2017. Clonal distribution and associated characteristics of Escherichia coli clinical and surveillance isolates from a military medical center. Diagn. Microbiol. Infect. Dis. 87:382–385.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
