Providencia
as an opportunistic pathogen can cause serious infection, and moreover the emergence of multi-drug-resistant
Providencia
strains poses a potentially life-threatening risk to public health. However, a comprehensive genomic study to reveal the population structure and dissemination of
Providencia
is still lacking. In this study, we conducted a genomic epidemiology analysis on the 580 global sequenced
Providencia
isolates, including 257 ones sequenced in this study (42 ones were fully sequenced). We established a genome sequence-based species classification scheme for
Providencia
, redefining the conventional 11
Providencia
species into seven genocomplexes that were further divided into 18 genospecies, providing an extensively updated reference for
Providencia
species discrimination based on the largest
Providencia
genome dataset to date. We then dissected the profile of antimicrobial resistance genes and the prevalence of multi-drug-resistant
Providencia
strains among these genocomplexes/genospecies, disclosing the presence of diverse and abundant antimicrobial resistance genes and high resistance ratios against multiple classes of drugs in
Providencia
. We further dissected the genetic basis for the spread of
bla
NDM-1
in
Providencia
.
bla
NDM-1
genes were mainly carried by five incompatible (Inc) groups of plasmids: IncC, IncW, Inc
pPROV114-NR
, Inc
pCHS4.1-3
, and Inc
pPrY2001
, and the last three were newly designated in this study. By tracking the spread of
bla
NDM-1
-carrying plasmids, IncC, Inc
pPROV114-NR
, Inc
pCHS4.1-3
, and Inc
pPrY2001
plasmids were found to be highly involved in parallel horizontal transfer or vertical clonal expansion of
bla
NDM-1
among
Providencia
. Overall, our study provided a comprehensive genomic view of species differentiation, antimicrobial resistance prevalence, and plasmid-mediated
bla
NDM-1
dissemination in
Providencia
.