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The Present and Future of Whole Genome Sequencing (WGS) and Whole Metagenome Sequencing (WMS) for Surveillance of Antimicrobial Resistant Microorganisms and Antimicrobial Resistance Genes across the Food Chain
 
 
Correction to Genes 2018, 9(5), 268.
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Correction: Oniciuc, E. A.; et al. The Present and Future of Whole Genome Sequencing (WGS) and Whole Metagenome Sequencing (WMS) for Surveillance of Antimicrobial Resistant Microorganisms and Antimicrobial Resistance Genes across the Food Chain. Genes 2018, 9, 268.

1
Faculty of Food Science and Engineering, Dunarea de Jos University of Galati, Galati 800008, Romania
2
Laboratory of Food Microbiology, Department of Food Technology, Alexander Technological Educational Institute of Thessaloniki, Thessaloniki T.K. 57400, Greece
3
Department of Food Hygiene and Technology and Institute of Food Science and Technology, Universidad de León, 24071 León, Spain
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Submission received: 19 June 2018 / Accepted: 19 June 2018 / Published: 25 June 2018
(This article belongs to the Special Issue Genetics and Genomics of Foodborne Pathogens)
The authors wish to make the following changes to their paper [1]. Due to an undetected mistake in the references management, certain errors appeared in the reference list and a reference was duplicated in Table 1. Consequently, three references have been changed as follows:
Reference [51] “51. Kumar, N.; Mariappan, V.; Baddam, R.; Lankapalli, A.K.; Shaik, S.; Goh, K.L.; Loke, M.F.; Perkins, T.; Benghezal, M.; Hasnain, S.E.; et al. Comparative Genomic Analysis of Helicobacter pylori from Malaysia Identifies Three Distinct Lineages Suggestive of Differential Evolution. Nucleic Acids Res. 2015, 43, 324–335.” has been replaced by: “51. Qumar, S.; Majid, M.; Kumar, N.; Tiwari, S.K.; Semmler, T.; Devi, S.; Baddam, R.; Hussain, A.; Shaik, S.; Ahmed, N. Genome Dynamics and Molecular Infection Epidemiology of Multidrug-Resistant Helicobacter pullorum Isolates Obtained from Broiler and Free-Range Chickens in India. Appl. Environ. Microbiol. 2017, 83, e02305-16.”
Reference [44] “44. Rehman, M.U.; Zhang, H.; Iqbal, M.K.; Mehmood, K.; Huang, S.; Nabi, F.; Luo, H.; Lan, Y.; Li, J. Antibiotic Resistance, Serogroups, Virulence Genes, and Phylogenetic Groups of Escherichia coli Isolated from Yaks with Diarrhea in Qinghai Plateau, China. Gut Pathog. 2017, 9, 1–11.” has been replaced by “44. Rehman, M.A.; Yin, X.; Lepp, D.; Laing, C.; Ziebell, K.; Talbot, G.; Topp, E.; Diarra, M.S. Genomic Analysis of Third Generation Cephalosporin Resistant Escherichia coli from Dairy Cow Manure. Vet. Sci. 2017, 4, 4, doi:10.3390/vetsci4040057.”
Reference [60] “60. Wang, W.; Baloch, Z.; Peng, Z.; Hu, Y.; Xu, J.; Fanning, S.; Li, F. Genomic Characterization of a Large Plasmid Containing a blaNDM-1 Gene Carried on Salmonella enterica Serovar Indiana C629 Isolate from China. BMC Infect. Dis. 2017, 17, 1–8.” has been replaced by “60. Wang, J.; Li, X.; Li, J.; Hurley, D.; Bai, X.; Yu, Z.; Cao, Y.; Wall, E.; Fanning, S.; Bai, L. Complete Genetic Analysis of a Salmonella enterica serovar Indiana Isolate Accompanying Four Plasmids Carrying mcr-1, ESBL and Other Resistance Genes in China. Vet. Microbiol. 2017, 210, 142–146, doi:10.1016/j.vetmic.2017.08.024.”
Two references have been added, as they were omitted in error:
Reference [66] in Table 1 was wrongly cited, therefore it has been substituted by the new reference [66] “66. Li, B.; Yang, X.; Tan, H.; Ke, B.; He, D.; Wang, H.; Chen, Q.; Ke, C.; Zhang, Y. Whole Genome Sequencing Analysis of Salmonella enterica Serovar Weltevreden Isolated from Human Stool and Contaminated Food Samples Collected from the Southern Coastal Area of China. Int. J. Food Microbiol. 2018, 266, 317–323, doi:10.1016/j.ijfoodmicro.2017.10.032.”
Reference [8] in Table 1 was wrongly cited, therefore it has been substituted by the new reference [71] “71. Flórez, A.B.; Mayo, B. Antibiotic Resistance-Susceptibility Profiles of Streptococcus thermophilus Isolated from Raw Milk and Genome Analysis of the Genetic Basis of Acquired Resistances. Front. Microbiol. 2017, 8, 2608, doi:10.3389/fmicb.2017.02608.”
Due to this correction, reference numbers were adjusted to follow a numerical order. In [1], the previous references [66] and [71] are now [139] and [72], respectively.
The 31st row from Table 1, about S. enterica with origin in Dairy cattle and humans, was eliminated because it was a duplicate of row 28; the corrected table is:
The authors would like to apologize for any inconvenience caused to the readers by these changes.

References

  1. Oniciuc, E.A.; Likotrafiti, E.; Alvarez-Molina, A.; Prieto, M.; Santos, J.A.; Alvarez-Ordóñez, A. The Present and Future of Whole Genome Sequencing (WGS) and Whole Metagenome Sequencing (WMS) for Surveillance of Antimicrobial Resistant Microorganisms and Antimicrobial Resistance Genes across the Food Chain. Genes 2018, 9, 268. [Google Scholar] [CrossRef] [PubMed]
Table 1. Main research studies published in recent years applying whole genome sequencing (WGS) to characterize antimicrobial resistance (AMR) in foodborne bacteria.
Table 1. Main research studies published in recent years applying whole genome sequencing (WGS) to characterize antimicrobial resistance (AMR) in foodborne bacteria.
ReferenceMicrobial SpeciesNumber of Isolates SequencedOriginMain Findings in Relation to AMR
[36]Aeromonas salmonicida101FishAll sequenced isolates harbored three AMR genes against beta-lactam antibiotics encoded on the chromosome.
Some isolates also harbored several other plasmid encoded resistance genes against trimethoprim, sulphonamide, and aminoglycoside antibiotics.
[37]Campylobacter spp.589Retail poultry meatThe following AMR genes were identified: tetO, blaOXA-61, aph(2″)-Ic, aph(2″)-If, aph(2″)-Ig, aph(3′)-III, ant(6)-1a, aadE, aph(3″)-VIIa, and Inu(C).
Mutations in housekeeping genes (gyrA at position 86, 23S rRNA at position 2074 and 2075) associated with AMR phenotypes were also identified.
[38]Campylobacter spp.114Humans, retail meats, and cecal samples from food production animalsEighteen resistance genes, including tet(O), blaOXA-61, catA, lnu(C), aph(2″)-Ib, aph(2″)-Ic, aph(2′)-If, aph(2″)-Ig, aph(2″)-Ih, aac(6′)-Ie-aph(2″)-Ia, aac(6′)-Ie-aph(2″)-If, aac(6′)-Im, aadE, sat4, ant(6′), aad9, aph(3′)-Ic, and aph(3′)-IIIa, and mutations in two housekeeping genes (gyrA and 23S rRNA), were identified.
[26]Campylobacter coli2Retail meatsA self-transmissible plasmid carrying multiple antibiotic resistance genes was identified, carrying genes encoding resistance to gentamicin, kanamycin, streptomycin, streptothricin, and tetracycline.
Gentamicin resistance was due to a phosphotransferase gene, aph(2″)-Ig, not described previously.
[39]Clostridium difficile40Human and porcine originAMR genotypes were characterized by resistance to tetracycline [tetM, tetA(P), tetB(P), and tetW], clindamycin/erythromycin (ermB), and aminoglycosides (aph3-III-Sat4A-ant6-Ia).
Resistance was mediated by clinically important mobile genetic elements, most notably Tn6194 (harboring ermB) and a novel variant of Tn5397 (harboring tetM).
[40]C. difficile2Ground porkIdentification of vancomycin (vanW, vanA, vanR, vanS, vex2, vex3, vncR, vncS); fluoroquinolones (gyrA and gyrB); tetracyclines (tetM, translation elongation factor G); beta-lactams (blaZ); and macrolides (macrolide efflux protein, macrolide glycosyltransferase) resistance genes, and multiple multidrug resistance efflux pump genes.
[31]Enterococcus spp.197Various animal and food sourcesResistance genotypes correlated with resistance phenotypes in 96.5% of cases for the 11 drugs investigated.
[21]Enterococcus faecalis, Enterococcus faecium, Escherichia coli, Salmonella enterica serovar Typhimurium200PigsHigh concordance (99.74%) between phenotypic and predicted antimicrobial susceptibility was observed.
Correlation between MLST type and resistance profiles was only observed in S. enterica serovar Typhimurium, where isolates belonging to sequence type (ST) 34 were more resistant than ST19 isolates.
[41]ESBL-producing Enterobacteriaceae24Fish and environmental samplesNine of eleven sequenced fish isolates had the blaCTX-M-15 gene, whereas 12/13 from environment carried blaCTX-M-15.
AMR genes encoding resistance to sulfonamides (sul1/sul2), tetracyclines [tet(A)/tet(B)], fluoroquinolones [e.g., aac(6′)-Ib-cr, qnrS1], aminoglycosides [e.g., aac(3)-lld, strB, strA], and trimethoprim (e.g., dfrA14) were detected.
[42]E. coli17Retail chicken meatAll strains carried an IncK plasmid with a blaCMY-2 gene.
[43]E. coli168Broilers and free-range retail poultry (meat/ceca)The prevalence rates of ESBL producing E. coli among broiler chicken were: meat 46%; ceca 40%. Whereas, those for free range chicken were: meat 15%; ceca 30%.
E. coli from broiler and free-range chicken exhibited varied prevalence rates for multi-drug resistance (meat 68%; ceca 64% and meat 8%; ceca 26%, respectively).
[44]E. coli18Dairy cow manureAll sequenced isolates carried at least one β-lactamase bla gene: TEM-1, TEM-81, CTX-M115, CTX-M15, OXA-1, or CMY-2.
Several other AMR genes were detected in the sequenced isolates and all of them harbored AMR plasmids belonging to classic Inc groups.
[45]E. coli16Swine farmblaNDM-5 and mcr-1 were located on two different plasmids, which showed 100% nucleotide identity in all 16 strains.
[46]E. coli26Humans, cows, pigs, horse, rabbit, goat, environments and foodA total of 39 plasmids were identified.
Eight plasmids carried resistance genes to aminoglycosides, carbapenems, penicillins, cephalosporins, chloramphenicol, dihydrofolate reductase inhibitors, sulfonamides, tetracyclines, and resistance to heavy metals.
Two plasmids carried six of these resistance genes and two novel IncHI2 plasmids were also identified.
[47]E. coli42Feedlot cattle70% of the cattle strains carried at least one AMR gene
[48]E. coli3Dairy cowsThe mcr-1 gene (linked to colistin resistance) coexisted with multiple resistance genes in a plasmid (pXGE1mcr)
[49]E. coli, Salmonella spp.463Retail meats and farm local samplesTo improve the concordance between genotypic and phenotypic data, it was proposed to reduce the phenotypic cut-off values for streptomycin to ≥32 µg mL−1 for both Salmonella and E. coli.
[50]Helicobacter pullorum4Chicken meatAMR-associated SNPs were detected (linked to resistance to fluoroquinolones, macrolides, and tetracyclines).
[51]H. pullorum11Broiler and free-range chickenWGS revealed the presence of five or six well characterized AMR genes, including those encoding a resistance-nodulation-division efflux pump
[30]Klebsiella pneumoniae7Pig and human samples at abbatoirsAMR genes associated with resistance to β-lactams, aminoglycosides, fluoroquinolones, macrolides, lincosamide, streptogramins, rifampicin, sulfonamides, trimethoprim, phenicols, and tetracycline were identified.
[29]K. pneumoniae44Chicken, turkey and pork meatMeat-source isolates were significantly more likely to be multidrug resistant and resistant to tetracycline and gentamicin than clinical isolates.
Four sequence types occurred among both meat-source and clinical isolates.
[52]Listeria monocytogenes2Ready-to-eat foodSeven antibiotic and efflux pump related genes which may confer resistance against lincomycin, erythromycin, fosfomycin, quinolones, tetracycline, penicillin, and macrolides were identified in the genomes of both strains.
[53]L. monocytogenes5Environments from pork processing plantsStrains of a particular sequence type were shown to contain the BAC resistance transposon Tn6188, conveying resistance to quaternary ammonium compounds.
[54]Proteus mirabilis8Food-producing animalsSeven integrative and conjugative elements were identical to ICEPmiJpn1, carrying the cephalosporinase gene blaCMY-2.
[55]Non-typhoidal Salmonella536Retail meatA total of 65 unique resistance genes, plus mutations in two structural resistance loci, were identified.
First finding of extended-spectrum β-lactamases (ESBLs) (blaCTX-M1 and blaSHV2a) in retail meat isolates of Salmonella in the United States.
[56]Non-typhoidal Salmonella1738Animal, food and human sourcesThe Minimum Inhibitory Concentration (MIC) predictions were correlated with the ResFinder database.
The genotypic cut-off values were established for 13 antimicrobials against Salmonella.
[20]Non-typhoidal Salmonella3491Received by Public Health England’s Gastrointestinal Bacteria Reference Unit from different origins for surveillance purposesDiscrepancies between phenotypic and genotypic profiles for one or more antimicrobials were detected for 76 isolates (2.18%).
Only 88/52,365 (0.17%) isolate/antimicrobial combinations were discordant.
Pan-susceptibility to antimicrobials was observed in 2190 isolates (62.73%).
[33]S. enterica90Dairy cattle and humansGenotypic prediction of phenotypic resistance resulted in a mean sensitivity of 97.2 and specificity of 85.2.
[57]S. enterica serovar Typhimurium984SwineMultiple genotypic resistance determinants were predominant, including resistance against ampicillin, streptomycin, sulfonamides, and tetracyclines.
Phenotypic resistance to enrofloxacin and ceftiofur was found in conjunction with the presence of plasmid-mediated AMR genes.
[58]S. enterica serovar Typhimurium 1Swine carcassThe following AMR genes were identified: tetA, aac3IIa, aadA1, strA, strB, blaTEM-1B, qnrE, sul1, drfA1, and floR.
[59]S. enterica serovar Heidelberg113Humans, abbatoir poultry and retail poultryCMY-2 plasmids, all belonging to incompatibility group I1, were identified in cefoxitin-resistant isolates.
Analysis of IncI1 plasmid sequences revealed high identity (95% to 99%) to a previously described plasmid (pCVM29188_101) found in S. enterica serovar Kentucky.
[60]S. enterica serovar Indiana1Poultry slaughterhouse24 multi-drug resistance (MDR) genes, located on 4 plasmids, were identified, including the mcr-1 gene (linked to colistin resistance).
[61]S. enterica serovar Infantis12Humans, food-producing animals and meatSome isolates harbored a conjugative megaplasmid (~280–320 Kb) which carried the ESBL gene blaCTX-M-1, and additional genes [tet(A), sul1, dfrA1 and dfrA14] mediating cefotaxime, tetracycline, sulfonamide, and trimethoprim resistance.
[62]S. enterica serovar Muenster2Dairy farm environmentsThe plasmid-mediated qnrB19 gene and IncR plasmid type were identified in both isolates.
[63]S. enterica serovar Typhimurium225Humans, animals, feed, and foodThe non-clinical use of narrow-spectrum penicillins (e.g., benzylpenicillin) might have favored the diffusion of plasmids carrying the blaTEM-1 gene in S. enterica serotype Typhimurium in the late 1950s.
[64]S. enterica serovar Typhimurium4Poultry and humansThe following AMR genes were identified: strA, strB, and aadA1 (aminoglycosides); blaTEM-1B (β-lactams); catA1 (phenicols); sul1 and sul2 (sulphonamides); tet B (tetracyclines); and dfrA1 (trimethoprim).
[65]S. enterica serovar Typhimurium and S. enterica serovar Kentucky2Chicken carcassesA total of five plasmids conveying AMR genes were found.
[66]S. enterica serovar Weltevreden44Human stool and contaminated food samplesAMR genes were only identified in eight isolates, linked to resistance to tetracycline, ciprofloxacin or ampicillin.
[67]Staphylococcus aureus66Retail meatsEleven spa types were represented.
The majority of MRSA (84.8%) possessed SCCmec IV.
[68]S. aureus9Pork, chicken and turkey meatMultiple resistance genes/mutations were detected.
All livestock-associated methicillin-resistant S. aureus (LA-MRSA) harbored tet(M)tet(K) and tet(L)), and only seven of these additionally harbored multi-drug resistance to beta-lactams, quinolones, and macrolides.
[69]S. aureus12Livestock animalsMost isolates harbored resistance genes to ≥3 antimicrobial classes in addition to β-lactams. Heavy metal resistance genes were detected in most European ccrC positive isolates, with >80% harboring czrC, encoding zinc and cadmium resistance.
[70]S. aureus15Bulk milkA divergent mecA homologue (mecALGA251), later named as mecC, was identified.
[71]Streptococcus thermophilus5Raw milktet(S) and ermB identified as determinants of AMR.
[72]Carbapenem-resistant bacteria28Dairy cattleIsolates included: 3 E. coli harboring blaCMY-2 and truncated ompF genes; 8 Aeromonas harboring blacphA-like genes; 1 Acinetobacter baumannii harboring a novel blaOXA gene (blaOXA-497); and 6 Pseudomonas with conserved domains of various carbapenemase-producing genes.

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Oniciuc, E.A.; Likotrafiti, E.; Alvarez-Molina, A.; Prieto, M.; Santos, J.A.; Alvarez-Ordóñez, A. Correction: Oniciuc, E. A.; et al. The Present and Future of Whole Genome Sequencing (WGS) and Whole Metagenome Sequencing (WMS) for Surveillance of Antimicrobial Resistant Microorganisms and Antimicrobial Resistance Genes across the Food Chain. Genes 2018, 9, 268. Genes 2018, 9, 315. https://0-doi-org.brum.beds.ac.uk/10.3390/genes9070315

AMA Style

Oniciuc EA, Likotrafiti E, Alvarez-Molina A, Prieto M, Santos JA, Alvarez-Ordóñez A. Correction: Oniciuc, E. A.; et al. The Present and Future of Whole Genome Sequencing (WGS) and Whole Metagenome Sequencing (WMS) for Surveillance of Antimicrobial Resistant Microorganisms and Antimicrobial Resistance Genes across the Food Chain. Genes 2018, 9, 268. Genes. 2018; 9(7):315. https://0-doi-org.brum.beds.ac.uk/10.3390/genes9070315

Chicago/Turabian Style

Oniciuc, Elena A., Eleni Likotrafiti, Adrián Alvarez-Molina, Miguel Prieto, Jesús A. Santos, and Avelino Alvarez-Ordóñez. 2018. "Correction: Oniciuc, E. A.; et al. The Present and Future of Whole Genome Sequencing (WGS) and Whole Metagenome Sequencing (WMS) for Surveillance of Antimicrobial Resistant Microorganisms and Antimicrobial Resistance Genes across the Food Chain. Genes 2018, 9, 268." Genes 9, no. 7: 315. https://0-doi-org.brum.beds.ac.uk/10.3390/genes9070315

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