Human colonization with Phytobacter co-harbouring blaIMP-4 and mcr-9.1 highlights its potential as emerging human pathogen.

Abstract

Phytobacter is a recently delineated, frequently misidentified genus within the order Enterobacterales. Following two rare cases of patient colonization with multidrug resistant Phytobacter in Ireland, this study presents a genus-wide genomic analysis that aims to define the pathogenic potential of Phytobacter species, with emphasis on their role as emerging human pathogens and reservoirs of carbapenemases. Two carbapenemase-encoding isolates were recovered from rectal swabs in Ireland in 2024 and were initially identified as Phytobacter by MALDI-ToF. Whole-genome sequencing with in silico species typing (dDDH, ANI) provided definitive taxonomic resolution. A genus-wide maximum-likelihood core-genome phylogeny was reconstructed, and the plasmidome and resistome were bioinformatically profiled across all available Phytobacter genomes. Phenotypic susceptibility of the Irish isolates was determined through minimum inhibitory concentration (MIC) testing. The Irish isolates (P. diazotrophicus E787336 and P. ursingii E980862) are the first reported Phytobacter strains carrying both plasmid-borne blaIMP-4 and mcr-9.1 in the genus. MIC testing confirmed resistance to aztreonam, aminoglycosides, cephalosporins, fluoroquinolones, and the {beta}-lactam/{beta}-lactamase inhibitor combination piperacillin-tazobactam. Across 34 Phytobacter genomes examined, 22 distinct plasmid replicon types were identified in 22 isolates, often shared across species. The genus-wide resistome encompassed 71 genes, more than half predicted to be acquired, with carbapenemases detected in 26.5% (9/34) of the genomes. In summary, Phytobacter harbors a diverse, plasmid-borne resistome including carbapenemases, with documented cases of human colonization and infection. These findings support its recognition as an emerging pathogen and reservoir of antimicrobial resistance, underscoring the need for improved clinical identification, genomic surveillance, and preparedness for limited treatment options. Author summarySince Phytobacter was first characterized in 2007, this bacterial genus has mainly been associated with plant growth promotion. More recently, however, increasing reports of human infections have raised concerns about its potential as emerging bacterial pathogen. These are further underscored by the description of multidrug resistant isolates capable to withstand different classes of antimicrobials, including carbapenems which are often used as a last line of treatment. Following the rare finding of multidrug resistant Phytobacter in two patients in Ireland, we combined bioinformatics and laboratory testing to characterize the antimicrobial resistance profile of this overlooked bacterial genus. Our results uncover the variety of resistance determinants, including to carbapenems, which is encoded in the genomes of Phytobacter. This shows its potential as hidden reservoir of drug resistance and emerging bacterial pathogen. We encourage improved clinical recognition and monitoring of Phytobacter to better anticipate infections with limited therapeutic options.