Stenotrophomonas maltophilia complex: insights into evolutionary relationships, global distribution and pathogenicity

Kun Li; Keyi Yu; Zhenzhou Huang; Xiao Liu; Li Mei; Xiaodong Ren; Xuemei Bai; He Gao; Zhiwen Sun; Xiaoning Liu; Duochun Wang

doi:10.3389/fcimb.2023.1325379

Stenotrophomonas maltophilia complex: insights into evolutionary relationships, global distribution and pathogenicity

Front Cell Infect Microbiol. 2024 Jan 10:13:1325379. doi: 10.3389/fcimb.2023.1325379. eCollection 2023.

Authors

Kun Li^{1

2}, Keyi Yu², Zhenzhou Huang³, Xiao Liu², Li Mei⁴, Xiaodong Ren^{1

2}, Xuemei Bai², He Gao², Zhiwen Sun², Xiaoning Liu¹, Duochun Wang²

Affiliations

¹ School of Public Health, Lanzhou University, Lanzhou, China.
² National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China.
³ Microbiology Laboratory, Hangzhou Center for Disease Control and Prevention, Hangzhou, China.
⁴ National Pathogen Resource Center, Chinese Center for Disease Control and Prevention, Beijing, China.

Abstract

Introduction: Stenotrophomonas maltophilia complex (Smc) comprises opportunistic Gram-negative bacilli responsible for various nosocomial infections. Limited data exists concerning its evolutionary lineage, global prevalence and pathogenicity.

Methods: We conducted an extensive genomic analysis on 734 Smc genomes, of which 90 were newly sequenced and isolated from different patients. The species composition and evolutionary relationships of Smc were examined using core protein sequence analysis. Pathogenicity evaluation was used by assays for swimming motility, biofilm formation and identification of virulence factors. The broth microdilution method was used to evaluate the drug resistance spectrum of clinical isolates.

Results: Phylogenetic analyses delineated 24 species-level clades, dominated by S. maltophilia (42.8%), S. sepilia (13.6%) and S. geniculata (9.9%). Geographically, strains were primarily distributed in Europe (34.2%), Asia (33.7%) and North America (24.0%), with intricate global distribution patterns. Meanwhile, 154 virulence-associated genes and 46 antimicrobial resistance genes within Smc were identified. These genes encoded span various functions, including motility, adherence, toxin, RND antibiotic efflux pumps, beta-lactamases and aminoglycoside-modifying enzymes. Moreover, significant variations were indicated in swimming motility and biofilm-forming capability across the different species, with S. sepilia exhibiting superior levels of both traits. Additionally, no statistically significant discrepancy was detected among Smc species to other antibiotics, despite the fact that all S. geniculata isolates were resistant to Ceftazidime and much higher than other species.

Conclusion: Our findings indicate the need to pay increased attention to other mainstream species of Smc besides S. maltophilia in order to better manage Smc-related infections and tailor effective treatment strategies.

Keywords: Stenotrophomonas maltophilia complex; biofilm; evolution; global distribution; pathogenicity; swimming motility.

Publication types

Research Support, U.S. Gov't, P.H.S.
Research Support, Non-U.S. Gov't

MeSH terms

Anti-Bacterial Agents / pharmacology
Biological Evolution
Humans
Phylogeny
Stenotrophomonas maltophilia* / genetics
Stenotrophomonas*
Virulence / genetics

Substances

Anti-Bacterial Agents

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Science and Technology Infrastructure of China (NPRC-32), the establishment of a national Shewanella standard strain (TS202303), the construction of protein fingerprints of rare pathogen (KFYJ-2022-039) and the Operation of Public Health Emergency Response Mechanisms-Infectious Disease Control and Prevention (102393220020020000029).