Genomic Analysis of Diverse EnvironmentalAcinetobacterIsolates Identifies Plasmids, Antibiotic Resistance Genes, and Capsular Polysaccharides Shared with Clinical Strains

Abstract

ABSTRACTAcinetobacter baumannii, an important pathogen known for its widespread antibiotic resistance, has been the focus of extensive research within its genus, primarily involving clinical isolates. Consequently, data on environmentalA. baumanniiand otherAcinetobacterspecies remain limited. Here, we utilised Illumina and Nanopore sequencing to analyse the genomes of tenAcinetobacterisolates representing six different species sourced from aquatic environments in South Australia. All ten isolates were phylogenetically distinct compared to clinical and other non-clinicalAcinetobacterstrains, often tens of thousands of SNPs from their nearest neighbours. Despite the genetic divergence, we identified pdifmodules (sections of mobilised DNA) carrying clinically important antimicrobial resistance genes in species other thanA. baumannii, including carbapenemaseoxa58,tetracycline resistance genetet(39) and macrolide resistance genesmsr(E)-mph(E).All of these pdifmodules were located on plasmids with high sequence homology to those circulating in globally distributedA. baumanniiST1 and ST2 clones. The environmentalA. baumanniiisolate characterised here (SAAb472; ST350) did not possess any native plasmids; however, it could capture two clinically important plasmids (pRAY and pACICU2) with high transfer frequencies. Furthermore,A. baumanniiSAAb472 possessed virulence genes and a capsular polysaccharide type analogous to clinical strains. Our findings highlight the potential for environmentalAcinetobacterspecies to acquire and disseminate clinically important antimicrobial resistance genes, underscoring the need for further research into the ecology and evolution of this important genus.IMPORTANCEAntimicrobial resistance (AMR) is a global threat to human, animal, and environmental health. Studying AMR in environmental bacteria is crucial to understand the emergence and dissemination of resistance genes and pathogens, and to identify potential reservoirs and transmission routes. This study provides novel insights into the genomic diversity and AMR potential of environmentalAcinetobacterspecies. By comparing the genomes of aquaticAcinetobacterisolates with clinical and non-clinical strains, we revealed that they are highly divergent yet carry pdifmodules that encode resistance to antibiotics commonly used in clinical settings. We also demonstrated that an environmentalA. baumanniiisolate can acquire clinically relevant plasmids and carries virulence factors similar to those of hospital-associated strains. These findings suggest that environmentalAcinetobacterspecies may serve as reservoirs and vectors of clinically important genes. Consequently, further research is warranted to comprehensively understand the ecology and evolution of this genus.