Phenotypic and genotypic characterization of Acinetobacter junii and Acinetobacter nosocomialis isolated from humans, animals, and the environment in Lagos, Nigeria

Abstract

The emerging threat of multidrug-resistant (MDR) Acinetobacter (A. ) species, coupled with limited data on its prevalence, resistance mechanisms, and genomic profiles in Nigeria, necessitates immediate study. This investigation characterized the microbial traits and genetic variation of Acinetobacter species isolated from human, animal, and environmental sources, with emphasis on resistance dynamics, virulence, inter-source relatedness and diversity in Lagos, Nigeria. From April 2023 to March 2024, 2835 samples were collected (1410 human, 1020 animal, and 405 environmental), processed, and the isolates were identified by classical microbiological methods. Further identification was carried out by Matrix-Assisted Laser Desorption Ionization-Time of Flight (MALDI-TOF) mass spectrometry and confirmed by Whole Genome Sequencing (WGS). Antibiotic susceptibility testing (AST) was assessed by the microdilution method using the MICRONAUT system. WGS data were utilized for analyzing virulence factors, antimicrobial resistance (AMR) determinants, and phylogenetic lineages. Nineteen isolates were confirmed as Acinetobacter by MALDI-TOF and WGS, of which 14 were A. nosocomialis and five were A. junii. The AST results revealed that both Acinetobacter species exhibited 100% resistance to cefotaxime and fosfomycin, while 100% of A. nosocomialis were resistant to chloramphenicol. Genomic analysis revealed that all A. nosocomialis isolates harbored 21 intrinsic AMR genes, including four distinct bla ADC variants and 17 efflux-related genes, which were all absent in A. junii. Moreover, A. nosocomialis harbored 68 virulence genes spanning seven mechanisms, compared to six virulence genes spanning five mechanisms in A. junii, with the absence of exotoxin and biofilm formation mechanisms. Both species have six conserved virulence-associated genes ompA, ACICURS00500, bfmR, pilG, pilT, and vgrG/tssI, and two distinct plasmids were exclusively detected in A. nosocomialis. Phylogenomic analysis demonstrated that both species formed distinct sub-clusters from different sources, suggesting shared evolutionary or transmission contexts. For example, five isolates (three A. nosocomialis from cattle nasal swab, human sputum, and abattoir effluent) and two A. junii from cattle rectal swab, and cattle nasal swab) form a distinct cluster differing by 15 SNP, indicating potential cross-species dynamics warranting deeper investigation. This study revealed the existence of A. nosocomialis and A. junii resistant to cefotaxime and fosfomycin in the One Health sector in Lagos. Both species were found to exhibit six conserved virulence genes linked to pathogenicity. Advanced molecular diagnostics is needed to monitor the emergence and spread of virulence and antibiotic-resistance in Acinetobacter species in Nigeria.