TY - JOUR
T1 - Global population structure of the Serratia marcescens complex and identification of hospital-adapted lineages in the complex
AU - Ono, Tomoyuki
AU - Taniguchi, Itsuki
AU - Nakamura, Keiji
AU - Nagano, Debora Satie
AU - Nishida, Ruriko
AU - Gotoh, Yasuhiro
AU - Ogura, Yoshitoshi
AU - Sato, Mitsuhiko P.
AU - Iguchi, Atsushi
AU - Murase, Kazunori
AU - Yoshimura, Dai
AU - Itoh, Takehiko
AU - Shima, Ayaka
AU - Dubois, Damien
AU - Oswald, Eric
AU - Shiose, Akira
AU - Gotoh, Naomasa
AU - Hayashi, Tetsuya
N1 - Funding Information:
This work was supported by KAKENHI from the Japan Society for the Promotion of Science (18K16175) granted to TH. DSN was supported by a Japanese Government Scholarship from MEXT (Ministry of Education, Culture, Sports, Science and Technology).
Publisher Copyright:
© 2022 The Authors.
PY - 2022
Y1 - 2022
N2 - Serratia marcescens is an important nosocomial pathogen causing various opportunistic infections, such as urinary tract infec-tions, bacteremia and sometimes even hospital outbreaks. The recent emergence and spread of multidrug-resistant (MDR) strains further pose serious threats to global public health. This bacterium is also ubiquitously found in natural environments, but the genomic differences between clinical and environmental isolates are not clear, including those between S. marcescens and its close relatives. In this study, we performed a large-scale genome analysis of S. marcescens and closely related species (referred to as the ‘S. marcescens complex’), including more than 200 clinical and environmental strains newly sequenced here. Our analysis revealed their phylogenetic relationships and complex global population structure, comprising 14 clades, which were defined based on whole-genome average nucleotide identity. Clades 10, 11, 12 and 13 corresponded to S. nematodiphila, S. marcescens sensu stricto, S. ureilytica and S. surfactantfaciens, respectively. Several clades exhibited distinct genome sizes and GC contents and a negative correlation of these genomic parameters was observed in each clade, which was associated with the acquisition of mobile genetic elements (MGEs), but different types of MGEs, plasmids or prophages (and other inte-grative elements), were found to contribute to the generation of these genomic variations. Importantly, clades 1 and 2 mostly comprised clinical or hospital environment isolates and accumulated a wide range of antimicrobial resistance genes, including various extended-spectrum β-lactamase and carbapenemase genes, and fluoroquinolone target site mutations, leading to a high proportion of MDR strains. This finding suggests that clades 1 and 2 represent hospital-adapted lineages in the S. marc-escens complex although their potential virulence is currently unknown. These data provide an important genomic basis for reconsidering the classification of this group of bacteria and reveal novel insights into their evolution, biology and differential importance in clinical settings.
AB - Serratia marcescens is an important nosocomial pathogen causing various opportunistic infections, such as urinary tract infec-tions, bacteremia and sometimes even hospital outbreaks. The recent emergence and spread of multidrug-resistant (MDR) strains further pose serious threats to global public health. This bacterium is also ubiquitously found in natural environments, but the genomic differences between clinical and environmental isolates are not clear, including those between S. marcescens and its close relatives. In this study, we performed a large-scale genome analysis of S. marcescens and closely related species (referred to as the ‘S. marcescens complex’), including more than 200 clinical and environmental strains newly sequenced here. Our analysis revealed their phylogenetic relationships and complex global population structure, comprising 14 clades, which were defined based on whole-genome average nucleotide identity. Clades 10, 11, 12 and 13 corresponded to S. nematodiphila, S. marcescens sensu stricto, S. ureilytica and S. surfactantfaciens, respectively. Several clades exhibited distinct genome sizes and GC contents and a negative correlation of these genomic parameters was observed in each clade, which was associated with the acquisition of mobile genetic elements (MGEs), but different types of MGEs, plasmids or prophages (and other inte-grative elements), were found to contribute to the generation of these genomic variations. Importantly, clades 1 and 2 mostly comprised clinical or hospital environment isolates and accumulated a wide range of antimicrobial resistance genes, including various extended-spectrum β-lactamase and carbapenemase genes, and fluoroquinolone target site mutations, leading to a high proportion of MDR strains. This finding suggests that clades 1 and 2 represent hospital-adapted lineages in the S. marc-escens complex although their potential virulence is currently unknown. These data provide an important genomic basis for reconsidering the classification of this group of bacteria and reveal novel insights into their evolution, biology and differential importance in clinical settings.
UR - http://www.scopus.com/inward/record.url?scp=85126852156&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85126852156&partnerID=8YFLogxK
U2 - 10.1099/mgen.0.000793
DO - 10.1099/mgen.0.000793
M3 - Article
C2 - 35315751
AN - SCOPUS:85126852156
SN - 2057-5858
VL - 8
JO - Microbial Genomics
JF - Microbial Genomics
IS - 3
M1 - 000793
ER -