Molecular characteristics of CTX-M β-lactamase-producing and quinolone-resistant Escherichia coli among deer in a popular tourist spot in Japan
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Introduction. Antimicrobial resistance (AMR) is a growing global concern. Clonal lineages of CTX-M β-lactamase-producing Escherichia coli (CTXE) and quinolone-resistant E. coli (QREC) were disseminated among the deer population in a famous tourist destination (Nara Park; NP) in Japan.
Hypothesis/gap statement. The molecular characteristics of CTXE or QREC isolates, which could pose a threat to public health, have not been elucidated.
Aim. This study aimed to characterize the genetic traits of CTXE and QREC isolates derived from NP deer and compare them with lineages prevalent worldwide.
Methodology. Sixteen CTXE and three QREC isolates recovered from NP deer faeces between 2018 and 2020 were analysed using whole-genome sequencing (WGS). For endemic lineages, phylogenetic trees were constructed against the isolates registered in the EnteroBase database using the core genome SNP scheme.
Results. The most prevalent lineage in NP deer was ST3580. Several pandemic lineages, such as sequence type (ST) 38, ST58 and ST117, were included. The QREC lineages prevalent among deer were designated as extra-intestinal pathogenic E. coli or uropathogenic E. coli (UPEC). Thirteen of the 24 antimicrobial resistance genes (ARGs) were considered high-risk ARG families. Chromosomal integration of bla CTX-M-15 was observed in all plasmid-negative isolates. Phylogenetic analysis suggested relationships between NP isolates and isolates sourced from the environment or poultry.
Conclusion. ST3580 has a high potential for clonal dissemination. Furthermore, multiple clinically relevant lineages of CTXE and QREC are endemic in NP deer; however, they could be less virulent than isolates belonging to the same lineages, which could cause severe infectious diseases. Further studies are required to investigate the relationship between chromosomal integration of plasmid-encoded genes and the stable propagation of AMR bacteria in wildlife and the environment.
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Thank you for your revised submission. I'm pleased to say, upon review of the changes, I am happy to Accept the manuscript. Thank you for choosing ACMI and we hope you consider us again in the future.
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The reviewers and I agree that the manuscript is valuable in progressing knowledge of AMR E. coli in this environment. The reviewers do provide important suggestions that I would like you to incorporate into a revision. Please pay particular attention to comments relating to the strength of your conclusions regarding human transmission in the absence of evidence for this.
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Comments to Author
This work by Ikushima and co-authors aims to characterize the genetic traits of CTXE and QREC isolates derived from deer in Nara Park Japan and to compare these isolates with lineages prevalent worldwide. Although this work has provided further knowledge about these isolates following their initial report in 2021 and 2023 [ref 5 and 9], some issues need to be addressed: Main text: 1. Although the investigated isolates were reported in previous work, clearer background information about them are needed in the method section for the readers to better follow this work. 2. For phylogenetic analysis method, the authors should include information on how additional genomes/isolates were selected from EnteroBase. Were all available genomes of ST3580 O8:H12 and ST117 O119:H4 included? If not, what was the …
Comments to Author
This work by Ikushima and co-authors aims to characterize the genetic traits of CTXE and QREC isolates derived from deer in Nara Park Japan and to compare these isolates with lineages prevalent worldwide. Although this work has provided further knowledge about these isolates following their initial report in 2021 and 2023 [ref 5 and 9], some issues need to be addressed: Main text: 1. Although the investigated isolates were reported in previous work, clearer background information about them are needed in the method section for the readers to better follow this work. 2. For phylogenetic analysis method, the authors should include information on how additional genomes/isolates were selected from EnteroBase. Were all available genomes of ST3580 O8:H12 and ST117 O119:H4 included? If not, what was the selection criteria used to obtain the genomes used for reconstructing the phylogeny and how many were selected? It will be also used full to include metadata in the tree presentation, such as the isolation time and country of origin. The authors should also provide more information on how cgSNP tree was reconstructed and what was the reference genome / parameters used. 3. Please define WWTP when it first was used in Line 184. 4. Not much comparison between NP isolates and global isolates was done as aimed by the authors, nor is there much discussion regarding this. Could the authors elaborate on the global prevalence of the lineages relevant to public health, such as ST38, ST58, and ST117 as identified by the authors? And what are the similarities and differences between the NP isolates and the global isolates? Tables and figure: 1. Table 1: Please provide note for "NAL" 2. Figure 1: please provide identity score for the aligned sequences/regions; Gene names in the text in the figure should be italicised. 3. Figure 2: Please indicate if the tree is rooted and what was the bootstrap value used.
Please rate the manuscript for methodological rigour
Satisfactory
Please rate the quality of the presentation and structure of the manuscript
Satisfactory
To what extent are the conclusions supported by the data?
Strongly support
Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?
No
Is there a potential financial or other conflict of interest between yourself and the author(s)?
No
If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?
Yes
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Comments to Author
Ikushima, Sugiyama and Tetsuo report carbapenemase producing and quinolone resistant E. coli disseminated in deer located in tourist hotspot Nara Park, Japan. They aim to characterise the genetic traits of these isolates and compare to others worldwide. They provide us with an overview of the situation in Nara Park as well it's context across a wider selection of E. coli. They have previously published the dissemination of these isolates but enhance this with whole-genome sequencing to look at gene content as well as relatedness. The authors probe at the idea of a threat of transmission to humans although this is not reflected in their findings. Their dataset consists of 19 isolates, of which the sequences are publicly available. The introduction is of suitable length and depth and is well referenced. …
Comments to Author
Ikushima, Sugiyama and Tetsuo report carbapenemase producing and quinolone resistant E. coli disseminated in deer located in tourist hotspot Nara Park, Japan. They aim to characterise the genetic traits of these isolates and compare to others worldwide. They provide us with an overview of the situation in Nara Park as well it's context across a wider selection of E. coli. They have previously published the dissemination of these isolates but enhance this with whole-genome sequencing to look at gene content as well as relatedness. The authors probe at the idea of a threat of transmission to humans although this is not reflected in their findings. Their dataset consists of 19 isolates, of which the sequences are publicly available. The introduction is of suitable length and depth and is well referenced. The methods outline the process sufficiently, with detail of any changes made. The results present the findings of both the phylogenetic analysis and the in depth gene analysis, in clear figures and tables. Comments: The data claimed to be sampled from between 2018 - 2020. In methods the two datasets are from 2018 and 2019. Furthermore, there is an isolate in Table 1 from 2020. I think it needs to be made clear where this isolate has come from and keep consistency in the years used throughout the paper. There is use of multiple abbreviations that are not defined including WWTP, CIP, NAL, ST. If the authors could expand this on each first occurrence. In the discussion, it needs to be addressed that although the isolates harbour resistance to clinically relevant antibiotics the majority of lineages found are not human pandemic lineages. Those that are associated with humans there were caveats such as ST38 isolates not exhibiting the traits of UPEC and the ST58s not showing a pathotype. There was no evidence presented for transmission or threat to public. Further comments: Line 35: Needs a reword - 'pose a threat to' or 'threaten' Line 44: ARG not defined. Line 55: Needs a reword - or maybe split into two sentences. 'Overuse or misuse of antimicrobials promotes the emergence and prevalence of AMR, migration of humans and animals, and inaccurate management of agricultural debris, which accelerates the spread of AMR.' This suggests Overuse or misuse of antimicrobials promotes the migration of humans. Line 76: β-lactamase producing not β-lactamases producing Line 77: Consider rewording the 'strong association between humans and deer' as perhaps in this context it is an interaction between the animals and humans. Line 98: Unclear whether this is 3 isolates or 9 isolates. Could it be one isolate from each of the three distinct pulsotypes Line 115/131/145/159/235: ST is generally the abbreviation for sequence type so the second type isn't necessary Line 131: Typo in serotype Line 147: The authors should consider an alternative word to contains. The five ST38 isolates did not contain the two serotypes rather the collection consists of two serotypes. Line 150: Could the authors confirm why the numbers are not listed in order? Line 160: Include ST types with listed isolates for clarity Line 177 & 178: Change 'at' to 'in', the insertion was in each of these isolates not at. Line 184: WWTP (abbreviation used with no long version) Line 234: 13 animals were positive. Could the authors confirm out of how many this was and consider including? Line 246: Do the authors mean prevalent rather than prevailed? Line 278: include 'ST' before 14709 Table 2: Misspelling of nutritional and metabolic in headers Figure 1: Are these figures shown 5' to 3'? If so, has there been an inversion of the transposon. Figure 2: It would make the figure clearer if the keys had the colours the same for categories that are in both. Isolates from this study could be highlighted to further emphasise their position.
Please rate the manuscript for methodological rigour
Good
Please rate the quality of the presentation and structure of the manuscript
Good
To what extent are the conclusions supported by the data?
Partially support
Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?
No
Is there a potential financial or other conflict of interest between yourself and the author(s)?
No
If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?
Yes
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