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Heuristic Mining of Hierarchical Genotypes and Accessory Genome Loci in Bacterial Populations
Published on: December 7, 2021
Global population structure of the Serratia marcescens complex and identification of hospital-adapted lineages in the
Tomoyuki Ono1,2, Itsuki Taniguchi1, Keiji Nakamura1
1Department of Bacteriology, Graduate School of Medical Sciences, Kyushu University, Higashi-ku, Fukuoka, 812-8582, Japan.
Abstract:
Serratia marcescens is an important nosocomial pathogen causing various opportunistic infections, such as urinary tract infections, 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 integrative 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. marcescens 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.
Insights
Multidrug-resistant Serratia marcescens strains are a global threat. Genomic analysis reveals hospital-adapted lineages (clades 1 and 2) with numerous antimicrobial resistance genes, distinct from environmental strains.
Area of Science:
- Microbiology
- Genomics
- Evolutionary Biology
Background:
- Serratia marcescens is a significant nosocomial pathogen responsible for opportunistic infections and hospital outbreaks.
- The emergence of multidrug-resistant (MDR) strains presents a growing public health concern.
- Genomic distinctions between clinical and environmental S. marcescens isolates and related species remain unclear.
Purpose of the Study:
- To conduct a large-scale genome analysis of the S. marcescens complex, including clinical and environmental strains.
- To elucidate phylogenetic relationships, population structure, and genomic variations within the S. marcescens complex.
- To identify potential hospital-adapted lineages and understand the genetic basis of antimicrobial resistance.
Main Methods:
- Whole-genome sequencing of over 200 clinical and environmental S. marcescens complex strains.
- Phylogenetic analysis based on whole-genome average nucleotide identity to define clades.
- Comparative genomic analysis to assess genome size, GC content, and mobile genetic element acquisition.
Main Results:
- The S. marcescens complex comprises 14 distinct clades, with specific clades identified as S. nematodiphila, S. marcescens sensu stricto, S. ureilytica, and S. surfactantfaciens.
- Genome size and GC content varied across clades, negatively correlated and influenced by mobile genetic elements like plasmids and prophages.
- Clades 1 and 2, predominantly clinical/hospital isolates, possess extensive antimicrobial resistance genes and fluoroquinolone resistance mutations, indicating MDR potential and hospital adaptation.
Conclusions:
- Genomic analysis provides a framework for reclassifying the S. marcescens complex.
- Hospital-adapted lineages (clades 1 and 2) have accumulated significant antimicrobial resistance genes.
- These findings offer insights into the evolution, biology, and clinical relevance of S. marcescens complex bacteria.
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