The ICU environment contributes to the endemicity of the “
Serratia marcescens
complex” in the hospital setting
Authors: Aracil-Gisbert Sonia , Fernández-De-Bobadilla Miguel D. , Guerra-Pinto Natalia , Serrano-Calleja Silvia , Pérez-Cobas Ana Elena , Soriano Cruz , de Pablo Raúl , Lanza Val F. , Pérez-Viso Blanca , Reuters Sandra , Hasman Henrik , Cantón Rafael , Baquero Fernando , Coque Teresa M. 
Published: April 2024

ABSTRACT

Serratia marcescens
is an opportunistic pathogen historically associated with sudden outbreaks in intensive care units (ICUs) and the spread of carbapenem-resistant genes. However, the ecology of
S. marcescens
populations in the hospital ecosystem remains largely unknown. We combined epidemiological information of 1,432
Serratia
spp. isolates collected from sinks of a large ICU that underwent demographic and operational changes (2019–2021) and 99 non-redundant outbreak/non-outbreak isolates from the same hospital (2003–2019) with 165 genomic data. These genomes were grouped into clades (1–4) and subclades (A and B) associated with distinct species:
Serratia nematodiphila
(1A),
S. marcescens
(1B),
Serratia bockelmannii
(2A),
Serratia ureilytica
(2B),
S. marcescens
/
Serratia nevei
(3), and
S. nevei
(4A and 4B). They may be classified into an
S. marcescens
complex (SMC) due to the similarity between/within subclades (average nucleotide identity >95%–98%), with clades 3 and 4 predominating in our study and publicly available databases. Chromosomal AmpC β-lactamase with unusual basal-like expression and prodigiosin-lacking species contrasted classical features of
Serratia
. We found persistent and coexisting clones in sinks of subclades 4A (ST92 and ST490) and 4B (ST424), clonally related to outbreak isolates carrying
bla
VIM-1
or
bla
OXA-48
on prevalent IncL/pB77-CPsm plasmids from our hospital since 2017. The distribution of SMC populations in ICU sinks and patients reflects how
Serratia
species acquire, maintain, and enable plasmid evolution in both “source” (permanent, sinks) and “sink” (transient, patients) hospital patches. The results contribute to understanding how water sinks serve as reservoirs of
Enterobacterales
clones and plasmids that enable the persistence of carbapenemase genes in healthcare settings, potentially leading to outbreaks and/or hospital-acquired infections.

IMPORTANCE

The “hospital environment,” including sinks and surfaces, is increasingly recognized as a reservoir for bacterial species, clones, and plasmids of high epidemiological concern. Available studies on
Serratia
epidemiology have focused mainly on outbreaks of multidrug-resistant species, overlooking local longitudinal analyses necessary for understanding the dynamics of opportunistic pathogens and antibiotic-resistant genes within the hospital setting. This long-term genomic comparative analysis of
Serratia
isolated from the ICU environment with isolates causing nosocomial infections and/or outbreaks within the same hospital revealed the coexistence and persistence of
Serratia
populations in water reservoirs. Moreover, predominant sink strains may acquire highly conserved and widely distributed plasmids carrying carbapenemase genes, such as the prevalent IncL-pB77-CPsm (pOXA48), persisting in ICU sinks for years. The work highlights the relevance of ICU environmental reservoirs in the endemicity of certain opportunistic pathogens and resistance mechanisms mainly confined to hospitals.