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Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes

INTRODUCTION: Non-baumannii Acinetobacter species are increasingly isolated in the clinical setting and the environment. The aim of the present study was to analyze a genome database of 837 Acinetobacter spp. isolates, which included 798 non-baumannii Acinetobacter genomes, in order to define the co...

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Autores principales: Migliaccio, Antonella, Bray, James, Intoccia, Michele, Stabile, Maria, Scala, Giovanni, Jolley, Keith A., Brisse, Sylvain, Zarrilli, Raffaele
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10620307/
https://www.ncbi.nlm.nih.gov/pubmed/37928684
http://dx.doi.org/10.3389/fmicb.2023.1264030
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author Migliaccio, Antonella
Bray, James
Intoccia, Michele
Stabile, Maria
Scala, Giovanni
Jolley, Keith A.
Brisse, Sylvain
Zarrilli, Raffaele
author_facet Migliaccio, Antonella
Bray, James
Intoccia, Michele
Stabile, Maria
Scala, Giovanni
Jolley, Keith A.
Brisse, Sylvain
Zarrilli, Raffaele
author_sort Migliaccio, Antonella
collection PubMed
description INTRODUCTION: Non-baumannii Acinetobacter species are increasingly isolated in the clinical setting and the environment. The aim of the present study was to analyze a genome database of 837 Acinetobacter spp. isolates, which included 798 non-baumannii Acinetobacter genomes, in order to define the concordance of classification and discriminatory power of 7-gene MLST, 53-gene MLST, and single-nucleotide polymorphism (SNPs) phylogenies. METHODS: Phylogenies were performed on Pasteur Multilocus Sequence Typing (MLST) or ribosomal Multilocus Sequence Typing (rMLST) concatenated alleles, or SNPs extracted from core genome alignment. RESULTS: The Pasteur MLST scheme was able to identify and genotype 72 species in the Acinetobacter genus, with classification results concordant with the ribosomal MLST scheme. The discriminatory power and genotyping reliability of the Pasteur MLST scheme were assessed in comparison to genome-wide SNP phylogeny on 535 non-baumannii Acinetobacter genomes assigned to Acinetobacter pittii, Acinetobacter nosocomialis, Acinetobacter seifertii, and Acinetobacter lactucae (heterotypic synonym of Acinetobacter dijkshoorniae), which were the most clinically relevant non-baumannii species of the A. baumannii group. The Pasteur MLST and SNP phylogenies were congruent at Robinson-Fould and Matching cluster tests and grouped genomes into four and three clusters in A. pittii, respectively, and one each in A. seifertii. Furthermore, A. lactucae genomes were grouped into one cluster within A. pittii genomes. The SNP phylogeny of A. nosocomialis genomes showed a heterogeneous population and did not correspond to the Pasteur MLST phylogeny, which identified two recombinant clusters. The antimicrobial resistance genes belonging to at least three different antimicrobial classes were identified in 91 isolates assigned to 17 distinct species in the Acinetobacter genus. Moreover, the presence of a class D oxacillinase, which is a naturally occurring enzyme in several Acinetobacter species, was found in 503 isolates assigned to 35 Acinetobacter species. CONCLUSION: In conclusion, Pasteur MLST phylogeny of non-baumannii Acinetobacter isolates coupled with in silico detection of antimicrobial resistance makes it important to study the population structure and epidemiology of Acinetobacter spp. isolates.
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spelling pubmed-106203072023-11-03 Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes Migliaccio, Antonella Bray, James Intoccia, Michele Stabile, Maria Scala, Giovanni Jolley, Keith A. Brisse, Sylvain Zarrilli, Raffaele Front Microbiol Microbiology INTRODUCTION: Non-baumannii Acinetobacter species are increasingly isolated in the clinical setting and the environment. The aim of the present study was to analyze a genome database of 837 Acinetobacter spp. isolates, which included 798 non-baumannii Acinetobacter genomes, in order to define the concordance of classification and discriminatory power of 7-gene MLST, 53-gene MLST, and single-nucleotide polymorphism (SNPs) phylogenies. METHODS: Phylogenies were performed on Pasteur Multilocus Sequence Typing (MLST) or ribosomal Multilocus Sequence Typing (rMLST) concatenated alleles, or SNPs extracted from core genome alignment. RESULTS: The Pasteur MLST scheme was able to identify and genotype 72 species in the Acinetobacter genus, with classification results concordant with the ribosomal MLST scheme. The discriminatory power and genotyping reliability of the Pasteur MLST scheme were assessed in comparison to genome-wide SNP phylogeny on 535 non-baumannii Acinetobacter genomes assigned to Acinetobacter pittii, Acinetobacter nosocomialis, Acinetobacter seifertii, and Acinetobacter lactucae (heterotypic synonym of Acinetobacter dijkshoorniae), which were the most clinically relevant non-baumannii species of the A. baumannii group. The Pasteur MLST and SNP phylogenies were congruent at Robinson-Fould and Matching cluster tests and grouped genomes into four and three clusters in A. pittii, respectively, and one each in A. seifertii. Furthermore, A. lactucae genomes were grouped into one cluster within A. pittii genomes. The SNP phylogeny of A. nosocomialis genomes showed a heterogeneous population and did not correspond to the Pasteur MLST phylogeny, which identified two recombinant clusters. The antimicrobial resistance genes belonging to at least three different antimicrobial classes were identified in 91 isolates assigned to 17 distinct species in the Acinetobacter genus. Moreover, the presence of a class D oxacillinase, which is a naturally occurring enzyme in several Acinetobacter species, was found in 503 isolates assigned to 35 Acinetobacter species. CONCLUSION: In conclusion, Pasteur MLST phylogeny of non-baumannii Acinetobacter isolates coupled with in silico detection of antimicrobial resistance makes it important to study the population structure and epidemiology of Acinetobacter spp. isolates. Frontiers Media S.A. 2023-10-19 /pmc/articles/PMC10620307/ /pubmed/37928684 http://dx.doi.org/10.3389/fmicb.2023.1264030 Text en Copyright © 2023 Migliaccio, Bray, Intoccia, Stabile, Scala, Jolley, Brisse and Zarrilli. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Migliaccio, Antonella
Bray, James
Intoccia, Michele
Stabile, Maria
Scala, Giovanni
Jolley, Keith A.
Brisse, Sylvain
Zarrilli, Raffaele
Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes
title Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes
title_full Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes
title_fullStr Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes
title_full_unstemmed Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes
title_short Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes
title_sort phylogenomics of acinetobacter species and analysis of antimicrobial resistance genes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10620307/
https://www.ncbi.nlm.nih.gov/pubmed/37928684
http://dx.doi.org/10.3389/fmicb.2023.1264030
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