Comparative genomic analysis of clinical Acinetobacter nosocomialis isolates from Terengganu, Malaysia led to the discovery of a novel tetracycline-resistant plasmid

Farahiyah Mohd Rani; Soo Sum Lean; Nor Iza A Rahman; Salwani Ismail; Ahmed Ghazi Alattraqchi; Malik Amonov; David W. Cleary; Stuart Clarke; Chew Chieng Yeo

doi:10.1016/j.jgar.2022.08.019

Comparative genomic analysis of clinical Acinetobacter nosocomialis isolates from Terengganu, Malaysia led to the discovery of a novel tetracycline-resistant plasmid

Farahiyah Mohd Rani, Soo Sum Lean, Nor Iza A Rahman, Salwani Ismail, Ahmed Ghazi Alattraqchi, Malik Amonov, David W. Cleary, Stuart Clarke, Chew Chieng Yeo^*

^*Corresponding author for this work

Microbiology and Infection

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Abstract

Objectives: To analyse the genome sequences of four archival Acinetobacter nosocomialis clinical isolates (designated AC13, AC15, AC21 and AC25) obtained from Terengganu, Malaysia in 2011 to determine their genetic relatedness and basis of antimicrobial resistance.

Methods: Antimicrobial susceptibility profiles of the A. nosocomialis isolates were determined by disk diffusion. Genome sequencing was performed using the Illumina NextSeq platform.

Results: The four A. nosocomialis isolates were cefotaxime resistant whereas three isolates (namely, AC13, AC15 and AC25) were tetracycline resistant. The carriage of the bla _ADC-255-encoded cephalosporinase gene is likely responsible for cefotaxime resistance in all four isolates. Phylogenetic analysis indicated that the three tetracycline-resistant isolates were closely related, with an average nucleotide identity of 99.9%, suggestive of nosocomial spread, whereas AC21 had an average nucleotide identity of 97.9% when compared to these three isolates. The tetracycline-resistant isolates harboured two plasmids: a 13476 bp Rep3-family plasmid of the GR17 group designated pAC13-1, which encodes the tetA(39) tetracycline-resistance gene, and pAC13-2, a 4872 bp cryptic PriCT-1-family plasmid of a new Acinetobacter plasmid group, GR60. The tetA(39) gene was in a 2 001 bp fragment flanked by XerC/XerD recombination sites characteristic of a mobile pdif module. Both plasmids also harboured mobilisation/transfer-related genes.

Conclusions: Genome sequencing of A. nosocomialis isolates led to the discovery of two novel plasmids, one of which encodes the tetA(39) tetracycline-resistant gene in a mobile pdif module. The high degree of genetic relatedness among the three tetracycline-resistant A. nosocomialis isolates is indicative of nosocomial transmission.

Original language	English
Pages (from-to)	104-109
Number of pages	6
Journal	Journal of Global Antimicrobial Resistance
Volume	31
Early online date	29 Aug 2022
DOIs	https://doi.org/10.1016/j.jgar.2022.08.019
Publication status	Published - Dec 2022

Bibliographical note

Funding Information:
This study was supported by the Fundamental Research Grant Scheme FRGS/1/2018/SKK11/UNISZA/01/1 from the Ministry of Higher Education Malaysia. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Ethical approval for the collection of Acinetobacter spp. isolates was obtained from the Malaysian Ministry of Health's Medical Research Ethics Council (approval no. NMRR-14-1650-23625-IIR). We thank Dr. Fatimah Haslina Abdullah and Dr. Norlela Othman of Hospital Sultanah Nur Zahirah, Kuala Terengganu, for the Acinetobacter nosocomialis strains used in this study.

Publisher Copyright:
© 2022 The Author(s)

Keywords

Acinetobacter nosocomialis
Plasmids
Tetracycline resistance
Whole genome sequence
pdif modules

ASJC Scopus subject areas

Microbiology
Immunology and Allergy
Immunology
Microbiology (medical)

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Rani, F. M., Lean, S. S., Rahman, N. I. A., Ismail, S., Alattraqchi, A. G., Amonov, M., Cleary, D. W., Clarke, S., & Yeo, C. C. (2022). Comparative genomic analysis of clinical Acinetobacter nosocomialis isolates from Terengganu, Malaysia led to the discovery of a novel tetracycline-resistant plasmid. Journal of Global Antimicrobial Resistance, 31, 104-109. https://doi.org/10.1016/j.jgar.2022.08.019

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title = "Comparative genomic analysis of clinical Acinetobacter nosocomialis isolates from Terengganu, Malaysia led to the discovery of a novel tetracycline-resistant plasmid",

abstract = "Objectives: To analyse the genome sequences of four archival Acinetobacter nosocomialis clinical isolates (designated AC13, AC15, AC21 and AC25) obtained from Terengganu, Malaysia in 2011 to determine their genetic relatedness and basis of antimicrobial resistance. Methods: Antimicrobial susceptibility profiles of the A. nosocomialis isolates were determined by disk diffusion. Genome sequencing was performed using the Illumina NextSeq platform. Results: The four A. nosocomialis isolates were cefotaxime resistant whereas three isolates (namely, AC13, AC15 and AC25) were tetracycline resistant. The carriage of the bla ADC-255-encoded cephalosporinase gene is likely responsible for cefotaxime resistance in all four isolates. Phylogenetic analysis indicated that the three tetracycline-resistant isolates were closely related, with an average nucleotide identity of 99.9%, suggestive of nosocomial spread, whereas AC21 had an average nucleotide identity of 97.9% when compared to these three isolates. The tetracycline-resistant isolates harboured two plasmids: a 13476 bp Rep3-family plasmid of the GR17 group designated pAC13-1, which encodes the tetA(39) tetracycline-resistance gene, and pAC13-2, a 4872 bp cryptic PriCT-1-family plasmid of a new Acinetobacter plasmid group, GR60. The tetA(39) gene was in a 2 001 bp fragment flanked by XerC/XerD recombination sites characteristic of a mobile pdif module. Both plasmids also harboured mobilisation/transfer-related genes. Conclusions: Genome sequencing of A. nosocomialis isolates led to the discovery of two novel plasmids, one of which encodes the tetA(39) tetracycline-resistant gene in a mobile pdif module. The high degree of genetic relatedness among the three tetracycline-resistant A. nosocomialis isolates is indicative of nosocomial transmission. ",

keywords = "Acinetobacter nosocomialis, Plasmids, Tetracycline resistance, Whole genome sequence, pdif modules",

author = "Rani, {Farahiyah Mohd} and Lean, {Soo Sum} and Rahman, {Nor Iza A} and Salwani Ismail and Alattraqchi, {Ahmed Ghazi} and Malik Amonov and Cleary, {David W.} and Stuart Clarke and Yeo, {Chew Chieng}",

note = "Funding Information: This study was supported by the Fundamental Research Grant Scheme FRGS/1/2018/SKK11/UNISZA/01/1 from the Ministry of Higher Education Malaysia. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Ethical approval for the collection of Acinetobacter spp. isolates was obtained from the Malaysian Ministry of Health's Medical Research Ethics Council (approval no. NMRR-14-1650-23625-IIR). We thank Dr. Fatimah Haslina Abdullah and Dr. Norlela Othman of Hospital Sultanah Nur Zahirah, Kuala Terengganu, for the Acinetobacter nosocomialis strains used in this study. Publisher Copyright: {\textcopyright} 2022 The Author(s)",

year = "2022",

month = dec,

doi = "10.1016/j.jgar.2022.08.019",

language = "English",

volume = "31",

pages = "104--109",

journal = "Journal of Global Antimicrobial Resistance",

issn = "2213-7165",

publisher = "Elsevier",

}

Rani, FM, Lean, SS, Rahman, NIA, Ismail, S, Alattraqchi, AG, Amonov, M, Cleary, DW, Clarke, S & Yeo, CC 2022, 'Comparative genomic analysis of clinical Acinetobacter nosocomialis isolates from Terengganu, Malaysia led to the discovery of a novel tetracycline-resistant plasmid', Journal of Global Antimicrobial Resistance, vol. 31, pp. 104-109. https://doi.org/10.1016/j.jgar.2022.08.019

Comparative genomic analysis of clinical Acinetobacter nosocomialis isolates from Terengganu, Malaysia led to the discovery of a novel tetracycline-resistant plasmid. / Rani, Farahiyah Mohd; Lean, Soo Sum; Rahman, Nor Iza A et al.
In: Journal of Global Antimicrobial Resistance, Vol. 31, 12.2022, p. 104-109.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Comparative genomic analysis of clinical Acinetobacter nosocomialis isolates from Terengganu, Malaysia led to the discovery of a novel tetracycline-resistant plasmid

AU - Rani, Farahiyah Mohd

AU - Lean, Soo Sum

AU - Rahman, Nor Iza A

AU - Ismail, Salwani

AU - Alattraqchi, Ahmed Ghazi

AU - Amonov, Malik

AU - Cleary, David W.

AU - Clarke, Stuart

AU - Yeo, Chew Chieng

N1 - Funding Information: This study was supported by the Fundamental Research Grant Scheme FRGS/1/2018/SKK11/UNISZA/01/1 from the Ministry of Higher Education Malaysia. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Ethical approval for the collection of Acinetobacter spp. isolates was obtained from the Malaysian Ministry of Health's Medical Research Ethics Council (approval no. NMRR-14-1650-23625-IIR). We thank Dr. Fatimah Haslina Abdullah and Dr. Norlela Othman of Hospital Sultanah Nur Zahirah, Kuala Terengganu, for the Acinetobacter nosocomialis strains used in this study. Publisher Copyright: © 2022 The Author(s)

PY - 2022/12

Y1 - 2022/12

N2 - Objectives: To analyse the genome sequences of four archival Acinetobacter nosocomialis clinical isolates (designated AC13, AC15, AC21 and AC25) obtained from Terengganu, Malaysia in 2011 to determine their genetic relatedness and basis of antimicrobial resistance. Methods: Antimicrobial susceptibility profiles of the A. nosocomialis isolates were determined by disk diffusion. Genome sequencing was performed using the Illumina NextSeq platform. Results: The four A. nosocomialis isolates were cefotaxime resistant whereas three isolates (namely, AC13, AC15 and AC25) were tetracycline resistant. The carriage of the bla ADC-255-encoded cephalosporinase gene is likely responsible for cefotaxime resistance in all four isolates. Phylogenetic analysis indicated that the three tetracycline-resistant isolates were closely related, with an average nucleotide identity of 99.9%, suggestive of nosocomial spread, whereas AC21 had an average nucleotide identity of 97.9% when compared to these three isolates. The tetracycline-resistant isolates harboured two plasmids: a 13476 bp Rep3-family plasmid of the GR17 group designated pAC13-1, which encodes the tetA(39) tetracycline-resistance gene, and pAC13-2, a 4872 bp cryptic PriCT-1-family plasmid of a new Acinetobacter plasmid group, GR60. The tetA(39) gene was in a 2 001 bp fragment flanked by XerC/XerD recombination sites characteristic of a mobile pdif module. Both plasmids also harboured mobilisation/transfer-related genes. Conclusions: Genome sequencing of A. nosocomialis isolates led to the discovery of two novel plasmids, one of which encodes the tetA(39) tetracycline-resistant gene in a mobile pdif module. The high degree of genetic relatedness among the three tetracycline-resistant A. nosocomialis isolates is indicative of nosocomial transmission.

AB - Objectives: To analyse the genome sequences of four archival Acinetobacter nosocomialis clinical isolates (designated AC13, AC15, AC21 and AC25) obtained from Terengganu, Malaysia in 2011 to determine their genetic relatedness and basis of antimicrobial resistance. Methods: Antimicrobial susceptibility profiles of the A. nosocomialis isolates were determined by disk diffusion. Genome sequencing was performed using the Illumina NextSeq platform. Results: The four A. nosocomialis isolates were cefotaxime resistant whereas three isolates (namely, AC13, AC15 and AC25) were tetracycline resistant. The carriage of the bla ADC-255-encoded cephalosporinase gene is likely responsible for cefotaxime resistance in all four isolates. Phylogenetic analysis indicated that the three tetracycline-resistant isolates were closely related, with an average nucleotide identity of 99.9%, suggestive of nosocomial spread, whereas AC21 had an average nucleotide identity of 97.9% when compared to these three isolates. The tetracycline-resistant isolates harboured two plasmids: a 13476 bp Rep3-family plasmid of the GR17 group designated pAC13-1, which encodes the tetA(39) tetracycline-resistance gene, and pAC13-2, a 4872 bp cryptic PriCT-1-family plasmid of a new Acinetobacter plasmid group, GR60. The tetA(39) gene was in a 2 001 bp fragment flanked by XerC/XerD recombination sites characteristic of a mobile pdif module. Both plasmids also harboured mobilisation/transfer-related genes. Conclusions: Genome sequencing of A. nosocomialis isolates led to the discovery of two novel plasmids, one of which encodes the tetA(39) tetracycline-resistant gene in a mobile pdif module. The high degree of genetic relatedness among the three tetracycline-resistant A. nosocomialis isolates is indicative of nosocomial transmission.

KW - Acinetobacter nosocomialis

KW - Plasmids

KW - Tetracycline resistance

KW - Whole genome sequence

KW - pdif modules

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DO - 10.1016/j.jgar.2022.08.019

M3 - Article

C2 - 36049733

SN - 2213-7165

VL - 31

SP - 104

EP - 109

JO - Journal of Global Antimicrobial Resistance

JF - Journal of Global Antimicrobial Resistance

ER -

Comparative genomic analysis of clinical Acinetobacter nosocomialis isolates from Terengganu, Malaysia led to the discovery of a novel tetracycline-resistant plasmid

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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