Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes

Antonella Migliaccio; James Bray; Michele Intoccia; Maria Stabile; Giovanni Scala; Keith A Jolley; Sylvain Brisse; Raffaele Zarrilli

doi:10.3389/fmicb.2023.1264030

Phylogenomics of Acinetobacter species and analysis of antimicrobial resistance genes

Front Microbiol. 2023 Oct 19:14:1264030. doi: 10.3389/fmicb.2023.1264030. eCollection 2023.

Authors

Antonella Migliaccio¹, James Bray², Michele Intoccia³, Maria Stabile^{1

4}, Giovanni Scala³, Keith A Jolley², Sylvain Brisse⁵, Raffaele Zarrilli¹

Affiliations

¹ Department of Public Health, University of Naples "Federico II", Naples, Italy.
² Department of Biology, University of Oxford, Oxford, United Kingdom.
³ Department of Biology, University of Naples Federico II, Naples, Italy.
⁴ Department of Chemical Sciences, University of Naples Federico II, Naples, Italy.
⁵ Institut Pasteur, Université Paris Cité, Biodiversity and Epidemiology of Bacterial Pathogens, Paris, France.

Abstract

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.

Keywords: Acinetobacter baumannii group; Acinetobacter spp.; Pasteur Multilocus Sequence Typing; antimicrobial resistance genes; maximum-likelihood phylogeny; ribosomal Multilocus Sequence Typing.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by grants from the Italian Ministry of University and Research (MUR): PRIN2017 (grant no. 2017SFBER to RZ) and PRIN2022 (grant no. 202288EJ8B to RZ).