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Fim3-dependent autoagglutination of Bordetella pertussis
Nao Otsuka1, Kentaro Koide2, Masataka Goto2
1Department of Bacteriology II, National Institute of Infectious Diseases, 4-7-1 Gakuen, Musashimurayama, Tokyo, 208-0011, Japan. notsuka@niid.go.jp.
Abstract:
Autoagglutination (Agg) of Bordetella pertussis is often observed in clinical laboratory. However, its causal factors and frequency in circulating strains are unknown. Repeated single colony isolation enabled us to detect an Agg- mutant in the supernatant of an Agg+ strain of B. pertussis. Whole-genome sequencing and immunoblot analysis disclosed that the Agg- mutant had a single C-deletion in its fim3 promoter region (Pfim3) which abolished Fim3 fimbriae production. A B. pertussis fim3-knock out mutant also lacked the Agg+ phenotype. Agg+ clinical isolates were detected a higher production of Fim3 than Fim3-producing Agg- isolates. B. pertussis is known to harbor multiple Pfim3 poly(C) lengths within a single strain culture and our newly developed PCR/LDR assay revealed that Agg+ isolates harbor the highest Pfim3 poly-14C abundance. We evaluated the frequency of autoagglutination in clinical B. pertussis isolates collected in Japan between 1994 and 2018 (n = 203). Fim3 production was confirmed for 190 isolates and 74.7% of them displayed the Agg+ phenotype. The Agg+ phenotype was strongly associated with Pfim3 poly-14C abundance. Taken together, our findings demonstrated that B. pertussis autoagglutination occurs in response to high Fim3 levels and the Agg+ strain has predominated in Japan over the past two decades.
Insights
Autoagglutination in Bordetella pertussis is caused by high Fim3 fimbriae production, linked to specific promoter variations. Agglutinating strains producing more Fim3 have predominated in Japan for over 20 years.
Area of Science:
- Microbiology
- Bacterial Pathogenesis
- Molecular Biology
Background:
- Autoagglutination (Agg) in Bordetella pertussis is a common laboratory observation, but its underlying causes and prevalence in circulating strains remain unclear.
- Understanding the factors contributing to Agg is crucial for accurate diagnosis and epidemiological surveillance of pertussis.
Purpose of the Study:
- To investigate the genetic and molecular basis of autoagglutination in Bordetella pertussis.
- To determine the frequency and characteristics of autoagglutinating strains in clinical isolates from Japan.
Main Methods:
- Single colony isolation to identify Agg-deficient mutants.
- Whole-genome sequencing and immunoblot analysis to identify genetic mutations.
- Development of a PCR/LDR assay to analyze Pfim3 poly(C) lengths.
- Phenotypic analysis of autoagglutination and Fim3 production in clinical isolates.
Main Results:
- A single C-deletion in the fim3 promoter region (Pfim3) was identified as abolishing Fim3 fimbriae production and the Agg+ phenotype.
- Fim3 production was significantly higher in Agg+ clinical isolates compared to Agg- isolates.
- Agg+ Bordetella pertussis isolates predominantly harbor the highest Pfim3 poly(C) abundance.
- Over two decades (1994-2018), 74.7% of 203 clinical isolates in Japan exhibited the Agg+ phenotype, strongly associated with Pfim3 poly(C) abundance.
Conclusions:
- Bordetella pertussis autoagglutination is directly linked to high Fim3 fimbriae levels, regulated by Pfim3 poly(C) length.
- Agg+ strains with high Fim3 production have predominated in Japan over the past two decades, suggesting a potential evolutionary advantage or epidemiological shift.
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