Whole-genome sequencing provides insights into a novel species: <i>Providencia hangzhouensis</i> associated with urinary tract infections

Abstract

<i>Providencia rettgeri</i> is a clinically significant opportunistic pathogen that is involved in urinary tract infections. Due to the resolution limitations of identification, distinguishing <i>P. rettgeri</i> from closely related species is challenging by commercial biochemical test systems. Here, we first reported a novel species, <i>Providencia hangzhouensis</i>, which had been misidentified as <i>P. rettgeri</i>. Exhibiting ≤91.97% average nucleotide identity (ANI) and ≤46.10% in silico DNA-DNA hybridization values with all known <i>Providencia</i> species, <i>P. hangzhouensis</i> falls well beneath the established species-defining thresholds. We conducted a population genomics analysis of <i>P. hangzhouensis</i> isolates worldwide. Our study revealed that <i>P. hangzhouensis</i> has emerged in many countries and has formed several transmission clusters. We found that <i>P. hangzhouensis</i> shared the highest ANI values (91.54% and 91.97%) with <i>P. rettgeri</i> and <i>P. huaxiensis</i>, respectively. The pan-genome analysis revealed that these three species possessed a similar component of pan-genomes. Two genes associated with metabolism, <i>folE2</i> and <i>ccmM</i>, were identified to be specific to <i>P. hangzhouensis</i>. Furthermore, we also observed that carbapenem-resistance genes frequently occur in <i>P. hangzhouensis</i> with the <i>bla</i>_IMP-27 being the most prevalent (46.15%; 36/78). The emergence of <i>P. hangzhouensis</i> is often accompanied by extended-spectrum β-lactamase and carbapenem-resistance genes, and calls for tailored surveillance of this species as a clinically relevant species in the future. IMPORTANCE Our study has identified and characterized a novel species, <i>Providencia hangzhouensis</i>, which is associated with urinary tract infections and was previously misidentified as <i>Providencia rettgeri</i>. Through this study, we have identified specific genes unique to <i>P. hangzhouensis</i>, which could serve as marker genes for rapid PCR identification. Additionally, our findings suggest that the emergence of <i>P. hangzhouensis</i> is often accompanied by extended-spectrum β-lactamase and carbapenem-resistance genes, emphasizing the need for attention to clinical management and the importance of accurate species identification and proper drug use.